Performance of abiotic stress-inducible synthetic promoters in genetically engineered hybrid poplar (Populus tremula × Populus alba)
Abstract
Abiotic stresses can cause significant damage to plants. For sustainable bioenergy crop production, it is critical to generate resistant crops to such stress. Engineering promoters to control the precise expression of stress resistance genes is a very effective way to address the problem. Here we developed stably transformed Populus tremula × Populus alba hybrid poplar (INRA 717-1B4) containing one-of-six s ynthetic d rought stress-inducible promoters (SDs; SD9-1, SD9-2, SD9-3, SD13-1, SD18-1, and SD18-3) identified previously by transient transformation assays. We screened green fluorescent protein (GFP) induction in poplar under osmotic stress conditions. Of six transgenic lines containing synthetic promoter, three lines (SD18-1, 9-2, and 9-3) had significant GFP expression in both salt and osmotic stress treatments. Each synthetic promoter employed heptamerized repeats of specific and short cis -regulatory elements (7 repeats of 7-8 bases). To verify whether the repeats of longer sequences can improve osmotic stress responsiveness, a transgenic poplar containing the synthetic promoter of the heptamerized entire SD9 motif (20 bases, containing all partial SD9 motifs) was generated and measured for GFP induction under osmotic stress. The heptamerized entire SD9 motif did not result in higher GFP expression than the shorter promoters consisting of heptamerized SD9-1, 9-2, and 9-3more »
- Authors:
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1893536
- Alternate Identifier(s):
- OSTI ID: 1900520
- Report Number(s):
- PNNL-SA-174829
Journal ID: ISSN 1664-462X; 1011939
- Grant/Contract Number:
- AC05-76RL01830; SC0018347
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Name: Frontiers in Plant Science Journal Volume: 13; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; synthetic biology; synthetic promoter; poplar; abiotic stress; cis-regulatory elements; bioenergy
Citation Formats
Yang, Yongil, Shao, Yuanhua, Chaffin, Timothy A., Lee, Jun Hyung, Poindexter, Magen R., Ahkami, Amir H., Blumwald, Eduardo, and Stewart, Jr, C. Neal. Performance of abiotic stress-inducible synthetic promoters in genetically engineered hybrid poplar (Populus tremula × Populus alba). Switzerland: N. p., 2022.
Web. doi:10.3389/fpls.2022.1011939.
Yang, Yongil, Shao, Yuanhua, Chaffin, Timothy A., Lee, Jun Hyung, Poindexter, Magen R., Ahkami, Amir H., Blumwald, Eduardo, & Stewart, Jr, C. Neal. Performance of abiotic stress-inducible synthetic promoters in genetically engineered hybrid poplar (Populus tremula × Populus alba). Switzerland. https://doi.org/10.3389/fpls.2022.1011939
Yang, Yongil, Shao, Yuanhua, Chaffin, Timothy A., Lee, Jun Hyung, Poindexter, Magen R., Ahkami, Amir H., Blumwald, Eduardo, and Stewart, Jr, C. Neal. Tue .
"Performance of abiotic stress-inducible synthetic promoters in genetically engineered hybrid poplar (Populus tremula × Populus alba)". Switzerland. https://doi.org/10.3389/fpls.2022.1011939.
@article{osti_1893536,
title = {Performance of abiotic stress-inducible synthetic promoters in genetically engineered hybrid poplar (Populus tremula × Populus alba)},
author = {Yang, Yongil and Shao, Yuanhua and Chaffin, Timothy A. and Lee, Jun Hyung and Poindexter, Magen R. and Ahkami, Amir H. and Blumwald, Eduardo and Stewart, Jr, C. Neal},
abstractNote = {Abiotic stresses can cause significant damage to plants. For sustainable bioenergy crop production, it is critical to generate resistant crops to such stress. Engineering promoters to control the precise expression of stress resistance genes is a very effective way to address the problem. Here we developed stably transformed Populus tremula × Populus alba hybrid poplar (INRA 717-1B4) containing one-of-six s ynthetic d rought stress-inducible promoters (SDs; SD9-1, SD9-2, SD9-3, SD13-1, SD18-1, and SD18-3) identified previously by transient transformation assays. We screened green fluorescent protein (GFP) induction in poplar under osmotic stress conditions. Of six transgenic lines containing synthetic promoter, three lines (SD18-1, 9-2, and 9-3) had significant GFP expression in both salt and osmotic stress treatments. Each synthetic promoter employed heptamerized repeats of specific and short cis -regulatory elements (7 repeats of 7-8 bases). To verify whether the repeats of longer sequences can improve osmotic stress responsiveness, a transgenic poplar containing the synthetic promoter of the heptamerized entire SD9 motif (20 bases, containing all partial SD9 motifs) was generated and measured for GFP induction under osmotic stress. The heptamerized entire SD9 motif did not result in higher GFP expression than the shorter promoters consisting of heptamerized SD9-1, 9-2, and 9-3 (partial SD9) motifs. This result indicates that shorter synthetic promoters (~50 bp) can be used for versatile control of gene expression in transgenic poplar. These synthetic promoters will be useful tools to engineer stress-resilient bioenergy tree crops in the future.},
doi = {10.3389/fpls.2022.1011939},
journal = {Frontiers in Plant Science},
number = ,
volume = 13,
place = {Switzerland},
year = {Tue Oct 18 00:00:00 EDT 2022},
month = {Tue Oct 18 00:00:00 EDT 2022}
}
https://doi.org/10.3389/fpls.2022.1011939
Works referenced in this record:
Gene activation by metazoan enhancers: Diverse mechanisms stimulate distinct steps of transcription
journal, July 2016
- Beagrie, Robert A.; Pombo, Ana
- BioEssays, Vol. 38, Issue 9
Plant abiotic stress: a prospective strategy of exploiting promoters as alternative to overcome the escalating burden
journal, August 2015
- Singhal, Parul; Jan, Arif Tasleem; Azam, Mudsser
- Frontiers in Life Science, Vol. 9, Issue 1
The regulatory landscape of Arabidopsis thaliana roots at single-cell resolution
journal, June 2021
- Dorrity, Michael W.; Alexandre, Cristina M.; Hamm, Morgan O.
- Nature Communications, Vol. 12, Issue 1
Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target
journal, December 2009
- Swiezewski, Szymon; Liu, Fuquan; Magusin, Andreas
- Nature, Vol. 462, Issue 7274
Eukaryotic core promoters and the functional basis of transcription initiation
journal, June 2018
- Haberle, Vanja; Stark, Alexander
- Nature Reviews Molecular Cell Biology, Vol. 19, Issue 10
Differentiation of core promoter architecture between plants and mammals revealed by LDSS analysis
journal, September 2007
- Yamamoto, Yoshiharu Y.; Ichida, Hiroyuki; Abe, Tomoko
- Nucleic Acids Research, Vol. 35, Issue 18
Genetic Transformation of Populus trichocarpa Genotype Nisqually-1: A Functional Genomic Tool for Woody Plants
journal, November 2006
- Song, Jingyuan; Lu, Shanfa; Chen, Zenn-Zong
- Plant and Cell Physiology, Vol. 47, Issue 11, p. 1582-1589
Deciphering eukaryotic gene-regulatory logic with 100 million random promoters
journal, December 2019
- de Boer, Carl G.; Vaishnav, Eeshit Dhaval; Sadeh, Ronen
- Nature Biotechnology, Vol. 38, Issue 1
Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root
journal, April 2021
- Zhang, Tian-Qi; Chen, Yu; Liu, Ye
- Nature Communications, Vol. 12, Issue 1
Plant synthetic biology innovations for biofuels and bioproducts
journal, October 2022
- Yang, Yongil; Chaffin, Timothy Alexander; Ahkami, Amir H.
- Trends in Biotechnology
A gene-editing/complementation strategy for tissue-specific lignin reduction while preserving biomass yield
journal, September 2021
- Yu, Hasi; Liu, Chang; Dixon, Richard A.
- Biotechnology for Biofuels, Vol. 14, Issue 1
Plant-produced biopharmaceuticals: A case of technical developments driving clinical deployment
journal, September 2016
- Lomonossoff, G. P.; DAoust, M. -A.
- Science, Vol. 353, Issue 6305
Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress
journal, June 2007
- RoyChoudhury, Aryadeep; Roy, Chaitali; Sengupta, Dibyendu N.
- Plant Cell Reports, Vol. 26, Issue 10
Core promoter sequence in yeast is a major determinant of expression level
journal, May 2015
- Lubliner, Shai; Regev, Ifat; Lotan-Pompan, Maya
- Genome Research, Vol. 25, Issue 7
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants
journal, May 2015
- Nakano, Yoshimi; Yamaguchi, Masatoshi; Endo, Hitoshi
- Frontiers in Plant Science, Vol. 6
Transgenic Poplar Designed for Biofuels
journal, September 2020
- Bryant, Nathan D.; Pu, Yunqiao; Tschaplinski, Timothy J.
- Trends in Plant Science, Vol. 25, Issue 9
Abiotic Stresses: General Defenses of Land Plants and Chances for Engineering Multistress Tolerance
journal, December 2018
- He, Mei; He, Cheng-Qiang; Ding, Nai-Zheng
- Frontiers in Plant Science, Vol. 9
Heat Stress-Mediated Constraints in Maize (Zea mays) Production: Challenges and Solutions
journal, April 2022
- El-Sappah, Ahmed H.; Rather, Shabir A.; Wani, Shabir Hussain
- Frontiers in Plant Science, Vol. 13
Genome-wide assessment of sequence-intrinsic enhancer responsiveness at single-base-pair resolution
journal, December 2016
- Arnold, Cosmas D.; Zabidi, Muhammad A.; Pagani, Michaela
- Nature Biotechnology, Vol. 35, Issue 2
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
DNA assembly standards: Setting the low-level programming code for plant biotechnology
journal, August 2018
- Vazquez-Vilar, Marta; Orzaez, Diego; Patron, Nicola
- Plant Science, Vol. 273
Paired-End Analysis of Transcription Start Sites in Arabidopsis Reveals Plant-Specific Promoter Signatures
journal, July 2014
- Morton, Taj; Petricka, Jalean; Corcoran, David L.
- The Plant Cell, Vol. 26, Issue 7
A cis-regulatory atlas in maize at single-cell resolution
journal, May 2021
- Marand, Alexandre P.; Chen, Zongliang; Gallavotti, Andrea
- Cell, Vol. 184, Issue 11
Transcriptional enhancers: from properties to genome-wide predictions
journal, March 2014
- Shlyueva, Daria; Stampfel, Gerald; Stark, Alexander
- Nature Reviews Genetics, Vol. 15, Issue 4
A Fruitful Decade Using Synthetic Promoters in the Improvement of Transgenic Plants
journal, November 2019
- Ali, Sajid; Kim, Won-Chan
- Frontiers in Plant Science, Vol. 10
Metazoan promoters: emerging characteristics and insights into transcriptional regulation
journal, March 2012
- Lenhard, Boris; Sandelin, Albin; Carninci, Piero
- Nature Reviews Genetics, Vol. 13, Issue 4
Rational design of minimal synthetic promoters for plants
journal, August 2020
- Cai, Yao-Min; Kallam, Kalyani; Tidd, Henry
- Nucleic Acids Research, Vol. 48, Issue 21
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Gene silencing in plants: A diversity of pathways
journal, December 2013
- Martínez de Alba, Angel Emilio; Elvira-Matelot, Emilie; Vaucheret, Hervé
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1829, Issue 12
Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor
journal, March 1999
- Kasuga, Mie; Liu, Qiang; Miura, Setsuko
- Nature Biotechnology, Vol. 17, Issue 3
Synthetic Switches and Regulatory Circuits in Plants
journal, January 2019
- Andres, Jennifer; Blomeier, Tim; Zurbriggen, Matias D.
- Plant Physiology, Vol. 179, Issue 3
Distinct Role of Core Promoter Architecture in Regulation of Light-Mediated Responses in Plant Genes
journal, April 2014
- Srivastava, Rakesh; Rai, Krishan Mohan; Srivastava, Meenal
- Molecular Plant, Vol. 7, Issue 4
Vessel-Specific Reintroduction of CINNAMOYL-COA REDUCTASE1 (CCR1) in Dwarfed ccr1 Mutants Restores Vessel and Xylary Fiber Integrity and Increases Biomass
journal, November 2017
- De Meester, Barbara; de Vries, Lisanne; Özparpucu, Merve
- Plant Physiology, Vol. 176, Issue 1
Translation regulation in plants: an interesting past, an exciting present and a promising future
journal, March 2017
- Merchante, Catharina; Stepanova, Anna N.; Alonso, Jose M.
- The Plant Journal, Vol. 90, Issue 4
Building the Plant SynBio Toolbox through Combinatorial Analysis of DNA Regulatory Elements
journal, July 2022
- Pfotenhauer, Alexander C.; Occhialini, Alessandro; Nguyen, Mary-Anne
- ACS Synthetic Biology, Vol. 11, Issue 8
Strength comparison between cold-inducible promoters of Arabidopsis cor15a and cor15b genes in potato and tobacco
journal, October 2013
- Li, Meng; Wang, Xiaohuan; Cao, Yang
- Plant Physiology and Biochemistry, Vol. 71
Multiple Classes of Transcription Factors Regulate the Expression of VASCULAR-RELATED NAC-DOMAIN7, a Master Switch of Xylem Vessel Differentiation
journal, September 2014
- Endo, Hitoshi; Yamaguchi, Masatoshi; Tamura, Taizo
- Plant and Cell Physiology, Vol. 56, Issue 2
The Q-System as a Synthetic Transcriptional Regulator in Plants
journal, March 2020
- Persad, Ramona; Reuter, D. Nikki; Dice, Lezlee T.
- Frontiers in Plant Science, Vol. 11
Identification of Plant Enhancers and Their Constituent Elements by STARR-seq in Tobacco Leaves
journal, May 2020
- Jores, Tobias; Tonnies, Jackson; Dorrity, Michael W.
- The Plant Cell, Vol. 32, Issue 7
The Expression of CARK1 or RCAR11 Driven by Synthetic Promoters Increases Drought Tolerance in Arabidopsis thaliana
journal, July 2018
- Ge, Hu; Li, Xiaoyi; Chen, Shisi
- International Journal of Molecular Sciences, Vol. 19, Issue 7
Transcript elongation factors: shaping transcriptomes after transcript initiation
journal, November 2014
- Van Lijsebettens, Mieke; Grasser, Klaus D.
- Trends in Plant Science, Vol. 19, Issue 11
Determinants of enhancer and promoter activities of regulatory elements
journal, October 2019
- Andersson, Robin; Sandelin, Albin
- Nature Reviews Genetics, Vol. 21, Issue 2
Plant synthetic biology
journal, May 2015
- Liu, Wusheng; Stewart, C. Neal
- Trends in Plant Science, Vol. 20, Issue 5
Imaging of multiple fluorescent proteins in canopies enables synthetic biology in plants
journal, December 2020
- Rigoulot, Stephen B.; Schimel, Tayler M.; Lee, Jun Hyung
- Plant Biotechnology Journal
Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants
journal, November 2006
- Sparkes, Imogen A.; Runions, John; Kearns, Anne
- Nature Protocols, Vol. 1, Issue 4
Synthetic promoter designs enabled by a comprehensive analysis of plant core promoters
journal, June 2021
- Jores, Tobias; Tonnies, Jackson; Wrightsman, Travis
- Nature Plants, Vol. 7, Issue 6
Rational design and testing of abiotic stress‐inducible synthetic promoters from poplar
cis
‐regulatory elements
journal, February 2021
- Yang, Yongil; Lee, Jun Hyung; Poindexter, Magen R.
- Plant Biotechnology Journal, Vol. 19, Issue 7
An atlas of active enhancers across human cell types and tissues
journal, March 2014
- Andersson, Robin; Gebhard, Claudia; Miguel-Escalada, Irene
- Nature, Vol. 507, Issue 7493
Design of orthogonal regulatory systems for modulating gene expression in plants
journal, May 2020
- Belcher, Michael S.; Vuu, Khanh M.; Zhou, Andy
- Nature Chemical Biology, Vol. 16, Issue 8
Specific Bacterial Pathogen Phytosensing Is Enabled by a Synthetic Promoter-Transcription Factor System in Potato
journal, April 2022
- Persad-Russell, Ramona; Mazarei, Mitra; Schimel, Tayler Marie
- Frontiers in Plant Science, Vol. 13
Innovation in plant-based transient protein expression for infectious disease prevention and preparedness
journal, February 2020
- Sainsbury, Frank
- Current Opinion in Biotechnology, Vol. 61
Synthetic promoters in planta
journal, August 2015
- Dey, Nrisingha; Sarkar, Shayan; Acharya, Sefali
- Planta, Vol. 242, Issue 5
Genome-wide mapping of autonomous promoter activity in human cells
journal, December 2016
- van Arensbergen, Joris; FitzPatrick, Vincent D.; de Haas, Marcel
- Nature Biotechnology, Vol. 35, Issue 2
Plant synthetic promoters and transcription factors
journal, February 2016
- Liu, Wusheng; Stewart, C. Neal
- Current Opinion in Biotechnology, Vol. 37
Genome sequence and genetic transformation of a widely distributed and cultivated poplar
journal, October 2018
- Ma, Jianchao; Wan, Dongshi; Duan, Bingbing
- Plant Biotechnology Journal, Vol. 17, Issue 2
Abiotic stress responses in plants
journal, September 2021
- Zhang, Huiming; Zhu, Jianhua; Gong, Zhizhong
- Nature Reviews Genetics, Vol. 23, Issue 2
Model-driven generation of artificial yeast promoters
journal, April 2020
- Kotopka, Benjamin J.; Smolke, Christina D.
- Nature Communications, Vol. 11, Issue 1
Systematic interrogation of human promoters
journal, January 2019
- Weingarten-Gabbay, Shira; Nir, Ronit; Lubliner, Shai
- Genome Research, Vol. 29, Issue 2
Systematic Localization of Common Disease-Associated Variation in Regulatory DNA
journal, September 2012
- Maurano, M. T.; Humbert, R.; Rynes, E.
- Science, Vol. 337, Issue 6099