Recombinant DNA modification of gibberellin metabolism alters growth rate and biomass allocation in Populus

Lu, Haiwei; Viswanath, Venkatesh; Ma, Cathleen; Etherington, Elizabeth; Dharmawardhana, Palitha; Shevchenko, Olga; Strauss, Steven H.; Pearce, David W.; Rood, Stewart B.; Busov, Victor

doi:10.1007/s11295-015-0952-0

Title: Recombinant DNA modification of gibberellin metabolism alters growth rate and biomass allocation in Populus

Journal Article · Fri Nov 13 00:00:00 EST 2015 · Tree Genetics & Genomes

DOI:https://doi.org/10.1007/s11295-015-0952-0· OSTI ID:1503042

Lu, Haiwei; Viswanath, Venkatesh; Ma, Cathleen; Etherington, Elizabeth; Dharmawardhana, Palitha; Shevchenko, Olga; Strauss, Steven H.; Pearce, David W.; Rood, Stewart B.; Busov, Victor

Overexpression of genes that modify gibberellin (GA) metabolism and signaling have been previously shown to produce trees with improved biomass production but highly disturbed development. In order to examine if more subtle types of genetic modification of GA could improve growth rate and modify tree architecture, we transformed a model poplar genotype (Populus tremula × P. alba) with eight genes, including two cisgenes (intact copies of native genes), four intragenes (modified copies of native genes), and two transgenes (from sexually incompatible species), and studied their effects under greenhouse and field conditions. In the greenhouse, four out of the eight tested genes produced a significant and often striking improvement of stem volume, and two constructs significantly modified the proportion of root or shoot biomass. Characterization of GA concentrations in the cisgenic population that had an additional copy of a poplar GA20-oxidase gene showed elevated concentrations of 13-hydroxylated GAs compared to wild-type poplars. In the field, we observed growth improvement for three of the six tested constructs, but it was significantly greater for only one of the constructs, a pRGL:GA20-oxidase intragene. The greenhouse and field responses were highly variable, possibly to due to cross-talk among the GA pathway and other stress response pathways, or due to interactions between the cisgenes and intragenes with highly similar endogenes. Our results indicate that extensive field trials, similar to those required for conventional breeding, will be critical to evaluating the value and pleiotropic effects of GA-modifying genes.

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Research Organization:: Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Oregon State Univ., Corvallis, OR (United States); Commonwealth Scientific and Industrial Research Organisation (CSIRO); Consortium for Plant Biotechnology Research, Inc. (CPBR), St. Simons Island, GA (United States); ArborGen, LLC, Ridgeville, SC (United States); US Dept. of Agriculture (USDA); Natural Sciences and Engineering Research Council of Canada (NSERC)

Grant/Contract Number:: FG02-06ER64185; FG02-05ER64113; GO12026-203A; 04412; 2003-04345; 2004-35300-14687

OSTI ID:: 1503042

Alternate ID(s):: OSTI ID: 1434578

Journal Information:: Tree Genetics & Genomes, Journal Name: Tree Genetics & Genomes Vol. 11 Journal Issue: 6; ISSN 1614-2942

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Germany

Language:: English

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Cited by: 6 works

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References (68)

A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome Gleave, Andrew P. Plant Molecular Biology, Vol. 20, Issue 6 https://doi.org/10.1007/BF00028910	journal	December 1992
The role of gibberellin signalling in plant responses to abiotic stress Colebrook, E. H.; Thomas, S. G.; Phillips, A. L. Journal of Experimental Biology, Vol. 217, Issue 1 https://doi.org/10.1242/jeb.089938	journal	December 2013
Gibberellin Signaling: Biosynthesis, Catabolism, and Response Pathways Olszewski, Neil; Sun, Tai-ping; Gubler, Frank The Plant Cell, Vol. 14, Issue suppl 1 https://doi.org/10.1105/tpc.010476	journal	May 2002
Gibberellin signaling in plants Daviere, J. -M.; Achard, P. Development, Vol. 140, Issue 6 https://doi.org/10.1242/dev.087650	journal	February 2013
Group I allergens of grass pollen as cell wall-loosening agents Cosgrove, D. J.; Bedinger, P.; Durachko, D. M. Proceedings of the National Academy of Sciences, Vol. 94, Issue 12 https://doi.org/10.1073/pnas.94.12.6559	journal	June 1997
The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway García-Hurtado, Noemí; Carrera, Esther; Ruiz-Rivero, Omar Journal of Experimental Botany, Vol. 63, Issue 16 https://doi.org/10.1093/jxb/ers229	journal	September 2012
Genetic containment of forest plantations Brunner, Amy M.; Li, Jingyi; DiFazio, Stephen P. Tree Genetics & Genomes, Vol. 3, Issue 2 https://doi.org/10.1007/s11295-006-0067-8	journal	January 2007
Root hair-specific EXPANSIN B genes have been selected for graminaceae root hairs Won, Su-Kyung; Choi, Sang-Bong; Kumari, Simple Molecules and Cells, Vol. 30, Issue 4 https://doi.org/10.1007/s10059-010-0127-7	journal	August 2010
(T RANS )G ENE S ILENCING IN P LANTS : How Many Mechanisms? Fagard, M.; Vaucheret, H. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 51, Issue 1 https://doi.org/10.1146/annurev.arplant.51.1.167	journal	June 2000
Gibberellin Homeostasis in Tobacco is Regulated by Gibberellin Metabolism Genes with Different Gibberellin Sensitivity Gallego-Giraldo, Lina; Ubeda-Tomás, Susana; Gisbert, Carmina Plant and Cell Physiology, Vol. 49, Issue 5 https://doi.org/10.1093/pcp/pcn042	journal	May 2008
Expansins and coleoptile elongation in wheat Gao, Qiang; Zhao, Meirong; Li, Feng Protoplasma, Vol. 233, Issue 1-2 https://doi.org/10.1007/s00709-008-0303-1	journal	August 2008
Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus Busov, Victor; Meilan, Richard; Pearce, David W. Planta, Vol. 224, Issue 2 https://doi.org/10.1007/s00425-005-0213-9	journal	January 2006
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Developing xylem-preferential expression of PdGA20ox1 , a gibberellin 20-oxidase 1 from Pinus densiflora , improves woody biomass production in a hybrid poplar Jeon, Hyung-Woo; Cho, Jin-Seong; Park, Eung-Jun Plant Biotechnology Journal, Vol. 14, Issue 4 https://doi.org/10.1111/pbi.12484	journal	October 2015
Gene stability in transgenic aspen ( Populus ). II. Molecular characterization of variable expression of transgene in wild and hybrid aspen Kumar, Sandeep; Fladung, Matthias Planta, Vol. 213, Issue 5 https://doi.org/10.1007/s004250100535	journal	September 2001
Ectopic expression of Expansin3 or Expansinβ1 causes enhanced hormone and salt stress sensitivity in Arabidopsis Kwon, Ye Rim; Lee, Hee Jin; Kim, Kyoung Heon Biotechnology Letters, Vol. 30, Issue 7 https://doi.org/10.1007/s10529-008-9678-5	journal	March 2008
Releasing the brakes of plant growth: how GAs shutdown DELLA proteins Achard, P.; Genschik, P. Journal of Experimental Botany, Vol. 60, Issue 4 https://doi.org/10.1093/jxb/ern301	journal	November 2008
Gibberellin biosynthesis and its regulation Hedden, Peter; Thomas, Stephen G. Biochemical Journal, Vol. 444, Issue 1 https://doi.org/10.1042/BJ20120245	journal	April 2012
Characterization of soybean β-expansin genes and their expression responses to symbiosis, nutrient deficiency, and hormone treatment Li, Xinxin; Zhao, Jing; Walk, Thomas C. Applied Microbiology and Biotechnology, Vol. 98, Issue 6 https://doi.org/10.1007/s00253-013-5240-z	journal	October 2013
Functional Analysis of SPINDLY in Gibberellin Signaling in Arabidopsis Silverstone, Aron L.; Tseng, Tong-Seung; Swain, Stephen M. Plant Physiology, Vol. 143, Issue 2 https://doi.org/10.1104/pp.106.091025	journal	December 2006
SPINDLY and GIGANTEA Interact and Act in Arabidopsis thaliana Pathways Involved in Light Responses, Flowering, and Rhythms in Cotyledon Movements Tseng, Tong-Seung; Salomé, Patrice A.; McClung, C. Robertson The Plant Cell, Vol. 16, Issue 6 https://doi.org/10.1105/tpc.019224	journal	May 2004
Gibberellins Regulate Lateral Root Formation in Populus through Interactions with Auxin and Other Hormones Gou, Jiqing; Strauss, Steven H.; Tsai, Chung Jui The Plant Cell, Vol. 22, Issue 3 https://doi.org/10.1105/tpc.109.073239	journal	March 2010
Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus Rodgers-Melnick, E.; Mane, S. P.; Dharmawardhana, P. Genome Research, Vol. 22, Issue 1 https://doi.org/10.1101/gr.125146.111	journal	October 2011
Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance: Transgenic poplar expressing Arabidopsis NDPK2 Kim, Yun-Hee; Kim, Myoung Duck; Choi, Young Im Plant Biotechnology Journal, Vol. 9, Issue 3 https://doi.org/10.1111/j.1467-7652.2010.00551.x	journal	March 2011
Molecular Cloning and Characterization of β -Expansin Gene Related to Root Hair Formation in Barley Kwasniewski, Miroslaw; Szarejko, Iwona Plant Physiology, Vol. 141, Issue 3 https://doi.org/10.1104/pp.106.078626	journal	May 2006
SPINDLY , a Negative Regulator of Gibberellic Acid Signaling, Is Involved in the Plant Abiotic Stress Response Qin, Feng; Kodaira, Ken-Suke; Maruyama, Kyonoshin Plant Physiology, Vol. 157, Issue 4 https://doi.org/10.1104/pp.111.187302	journal	October 2011
Abscisic Acid Synthesis and Response Finkelstein, Ruth The Arabidopsis Book, Vol. 11 https://doi.org/10.1199/tab.0166	journal	January 2013
Gibberellins and DELLAs: central nodes in growth regulatory networks Claeys, Hannes; De Bodt, Stefanie; Inzé, Dirk Trends in Plant Science, Vol. 19, Issue 4 https://doi.org/10.1016/j.tplants.2013.10.001	journal	April 2014
Mechanisms of Cross Talk between Gibberellin and Other Hormones Weiss, David; Ori, Naomi Plant Physiology, Vol. 144, Issue 3 https://doi.org/10.1104/pp.107.100370	journal	July 2007
Efficient transformation of Medicago truncatula cv. Jemalong using the hypervirulent Agrobacterium tumefaciens strain AGL1 Chabaud, M.; de Carvalho-Niebel, F.; Barker, D. G. Plant Cell Reports, Vol. 22, Issue 1 https://doi.org/10.1007/s00299-003-0649-y	journal	June 2003
The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis Shimada, Asako; Ueguchi-Tanaka, Miyako; Sakamoto, Tomoaki The Plant Journal, Vol. 48, Issue 3 https://doi.org/10.1111/j.1365-313X.2006.02875.x	journal	November 2006
Practical Applications of Manipulating Plant Architecture by Regulating Gibberellin Metabolism Bhattacharya, Anjanabha; Kourmpetli, Sofia; Davey, Michael R. Journal of Plant Growth Regulation, Vol. 29, Issue 2 https://doi.org/10.1007/s00344-009-9126-3	journal	December 2009
Alcohol-inducible gene expression in transgenic Populus Filichkin, S. A.; Meilan, R.; Busov, V. B. Plant Cell Reports, Vol. 25, Issue 7 https://doi.org/10.1007/s00299-005-0112-3	journal	February 2006
Intragenesis and cisgenesis as alternatives to transgenic crop development Holme, Inger Baeksted; Wendt, Toni; Holm, Preben Bach Plant Biotechnology Journal, Vol. 11, Issue 4 https://doi.org/10.1111/pbi.12055	journal	February 2013
Genetically engineered trees: Paralysis from good intentions Strauss, S. H.; Costanza, A.; Seguin, A. Science, Vol. 349, Issue 6250 https://doi.org/10.1126/science.aab0493	journal	August 2015
Gibberellin metabolism: new insights revealed by the genes Hedden, Peter; Phillips, Andrew L. Trends in Plant Science, Vol. 5, Issue 12 https://doi.org/10.1016/S1360-1385(00)01790-8	journal	December 2000
Abscisic Acid–Mediated Suppression of Systemic Acquired Resistance Signaling Hofmann, Nancy The Plant Cell, Vol. 20, Issue 6 https://doi.org/10.1105/tpc.108.200612	journal	June 2008
Gibberellin 20-Oxidase Gene OsGA20ox3 Regulates Plant Stature and Disease Development in Rice Qin, Xue; Liu, Jun Hua; Zhao, Wen Sheng Molecular Plant-Microbe Interactions, Vol. 26, Issue 2 https://doi.org/10.1094/MPMI-05-12-0138-R	journal	February 2013
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
Stability of transgenes in trees: expression of two reporter genes in poplar over three field seasons Li, J.; Brunner, A. M.; Meilan, R. Tree Physiology, Vol. 29, Issue 2 https://doi.org/10.1093/treephys/tpn028	journal	December 2008
Two expansins, EXP1 and EXPB2, are correlated with the growth and development of maize roots Kam, Min -Jeong; Yun, Hye Sup; Kaufman, Peter B. Journal of Plant Biology, Vol. 48, Issue 3 https://doi.org/10.1007/BF03030527	journal	September 2005
Gibberellins Signal Nuclear Import of PHOR1, a Photoperiod-Responsive Protein with Homology to Drosophila armadillo Amador, Virginia; Monte, Elena; Garcı́a-Martı́nez, José-Luis Cell, Vol. 106, Issue 3 https://doi.org/10.1016/S0092-8674(01)00445-7	journal	August 2001
Gibberellin Metabolism and its Regulation Yamaguchi, Shinjiro Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092804	journal	June 2008
Mixed effects models and extensions in ecology with R Zuur, Alain F.; Ieno, Elena N.; Walker, Neil Statistics for Biology and Health https://doi.org/10.1007/978-0-387-87458-6	book	January 2009
The Arabidopsis O -Linked N- Acetylglucosamine Transferase SPINDLY Interacts with Class I TCPs to Facilitate Cytokinin Responses in Leaves and Flowers Steiner, Evyatar; Efroni, Idan; Gopalraj, Manjula The Plant Cell, Vol. 24, Issue 1 https://doi.org/10.1105/tpc.111.093518	journal	January 2012
Drought tolerance through over-expression of the expansin gene TaEXPB23 in transgenic tobacco Li, Feng; Xing, Shichao; Guo, Qifang Journal of Plant Physiology, Vol. 168, Issue 9 https://doi.org/10.1016/j.jplph.2010.11.023	journal	June 2011
Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length Eriksson, Maria E.; Israelsson, Maria; Olsson, Olof Nature Biotechnology, Vol. 18, Issue 7 https://doi.org/10.1038/77355	journal	July 2000
Overexpression of the Gibberellin 20-Oxidase or Gibberellin 3-Oxidase gene from Torenia Fournieri Affecting Plant Morphology in Transgenic Tricyrtis sp. Otani, M.; Meguro, S.; Gondaira, H. Acta Horticulturae, Issue 1025 https://doi.org/10.17660/ActaHortic.2014.1025.2	journal	March 2014
Functional analysis of HvSPY, a negative regulator of GA response, in barley aleurone cells and Arabidopsis Filardo, Fiona; Robertson, Masumi; Singh, Davinder Pal Planta, Vol. 229, Issue 3 https://doi.org/10.1007/s00425-008-0843-9	journal	November 2008
Arabidopsis RGL1 Encodes a Negative Regulator of Gibberellin Responses Wen, Chi-Kuang; Chang, Caren The Plant Cell, Vol. 14, Issue 1 https://doi.org/10.1105/tpc.010325	journal	January 2002
PHOTOPERIOD RESPONSE 1 (PHOR1)-like Genes Regulate Shoot/root Growth, Starch Accumulation, and Wood Formation in Populus Zawaski, Christine; Ma, Cathleen; Strauss, Steven H. Journal of Experimental Botany, Vol. 63, Issue 15 https://doi.org/10.1093/jxb/ers217	journal	August 2012
SPINDLY, ERECTA, and Its Ligand STOMAGEN Have a Role in Redox-Mediated Cortex Proliferation in the Arabidopsis Root Cui, Hongchang; Kong, Danyu; Wei, Pengcheng Molecular Plant, Vol. 7, Issue 12 https://doi.org/10.1093/mp/ssu106	journal	December 2014
Convergent pathways of gibberellin A1 biosynthesis in Brassica Rood, Stewart; Hedden, Peter Plant Growth Regulation, Vol. 15, Issue 3 https://doi.org/10.1007/BF00029897	journal	November 1994
Manipulation of hormone biosynthetic genes in transgenic plants Hedden, Peter; Phillips, Andrew L. Current Opinion in Biotechnology, Vol. 11, Issue 2 https://doi.org/10.1016/S0958-1669(00)00071-9	journal	April 2000
Cloning and Overproduction of Gibberellin 3-Oxidase in Hybrid Aspen Trees. Effects on Gibberellin Homeostasis and Development Israelsson, Maria; Mellerowicz, Ewa; Chono, Makiko Plant Physiology, Vol. 135, Issue 1 https://doi.org/10.1104/pp.104.038935	journal	April 2004
Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates Matzke, M. A.; Mette, M. F.; Matzke, A. J. M. Plant Molecular Biology, Vol. 43, Issue 2/3, p. 401-415 https://doi.org/10.1023/A:1006484806925	journal	January 2000
Gibberellin-associated cisgenes modify growth, stature and wood properties in Populus: Gibberellin cisgenes in poplar Han, Katherine M.; Dharmawardhana, Palitha; Arias, Reneé S. Plant Biotechnology Journal, Vol. 9, Issue 2 https://doi.org/10.1111/j.1467-7652.2010.00537.x	journal	January 2011
Gibberellin Biosynthesis: Its Regulation by Endogenous and Environmental Signals Yamaguchi, S.; Kamiya, Y. Plant and Cell Physiology, Vol. 41, Issue 3 https://doi.org/10.1093/pcp/41.3.251	journal	March 2000
Reduction of Gibberellin by Low Temperature Disrupts Pollen Development in Rice Sakata, Tadashi; Oda, Susumu; Tsunaga, Yuta Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.113.234401	journal	February 2014
Ethylene Regulates Arabidopsis Development via the Modulation of DELLA Protein Growth Repressor Function Achard, Patrick; Vriezen, Wim H.; Van Der Straeten, Dominique The Plant Cell, Vol. 15, Issue 12 https://doi.org/10.1105/tpc.015685	journal	November 2003
Genes for control of plant stature and form Busov, Victor B.; Brunner, Amy M.; Strauss, Steven H. New Phytologist, Vol. 177, Issue 3 https://doi.org/10.1111/j.1469-8137.2007.02324.x	journal	February 2008
Gibberellins in shoots and developing capsules of Populus species Pearce, David W.; Hutt, Oliver E.; Rood, Stewart B. Phytochemistry, Vol. 59, Issue 6 https://doi.org/10.1016/S0031-9422(02)00009-2	journal	March 2002
Altered Expression of SPINDLY Affects Gibberellin Response and Plant Development Swain, Stephen M.; Tseng, Tong-seung; Olszewski, Neil E. Plant Physiology, Vol. 126, Issue 3 https://doi.org/10.1104/pp.126.3.1174	journal	July 2001
Tissue-specific expression of Populus C19 GA 2-oxidases differentially regulate above- and below-ground biomass growth through control of bioactive GA concentrations Gou, Jiqing; Ma, Cathleen; Kadmiel, Mahita New Phytologist, Vol. 192, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03837.x	journal	August 2011
Listening to the silent genes: transgene silencing, gene regulation and pathogen control Kooter, J. Trends in Plant Science, Vol. 4, Issue 9 https://doi.org/10.1016/S1360-1385(99)01467-3	journal	September 1999
The role of SPY and its TPR domain in the regulation of gibberellin action throughout the life cycle of Petunia hybrida plants: Manipulation of SPY expression in petunia Izhaki, Anat; Swain, Stephen M.; Tseng, Tong-seung The Plant Journal, Vol. 28, Issue 2 https://doi.org/10.1046/j.1365-313X.2001.01144.x	journal	October 2001
Cisgenic plants are similar to traditionally bred plants: International regulations for genetically modified organisms should be altered to exempt cisgenesis Schouten, Henk J.; Krens, Frans A.; Jacobsen, Evert EMBO reports, Vol. 7, Issue 8 https://doi.org/10.1038/sj.embor.7400769	journal	August 2006
High Temperature-Induced Abscisic Acid Biosynthesis and Its Role in the Inhibition of Gibberellin Action in Arabidopsis Seeds Toh, Shigeo; Imamura, Akane; Watanabe, Asuka Plant Physiology, Vol. 146, Issue 3 https://doi.org/10.1104/pp.107.113738	journal	December 2007

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