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

Title: 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 » (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.« less

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}
}

Works referenced in this record:

Gene activation by metazoan enhancers: Diverse mechanisms stimulate distinct steps of transcription
journal, July 2016


Plant abiotic stress: a prospective strategy of exploiting promoters as alternative to overcome the escalating burden
journal, August 2015


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
  • DOI: 10.1038/s41467-021-23675-y

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
  • DOI: 10.1038/nature08618

Eukaryotic core promoters and the functional basis of transcription initiation
journal, June 2018


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
  • DOI: 10.1093/nar/gkm685

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
  • DOI: 10.1093/pcp/pcl018

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
  • DOI: 10.1038/s41587-019-0315-8

Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root
journal, April 2021


Plant synthetic biology innovations for biofuels and bioproducts
journal, October 2022


A gene-editing/complementation strategy for tissue-specific lignin reduction while preserving biomass yield
journal, September 2021


Plant-produced biopharmaceuticals: A case of technical developments driving clinical deployment
journal, September 2016


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
  • DOI: 10.1007/s00299-007-0371-2

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
  • DOI: 10.1101/gr.188193.114

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
  • DOI: 10.3389/fpls.2015.00288

Transgenic Poplar Designed for Biofuels
journal, September 2020


Abiotic Stresses: General Defenses of Land Plants and Chances for Engineering Multistress Tolerance
journal, December 2018


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
  • DOI: 10.3389/fpls.2022.879366

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
  • DOI: 10.1038/nbt.3739

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
  • DOI: 10.1038/nmeth.2089

DNA assembly standards: Setting the low-level programming code for plant biotechnology
journal, August 2018


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
  • DOI: 10.1105/tpc.114.125617

A cis-regulatory atlas in maize at single-cell resolution
journal, May 2021


Transcriptional enhancers: from properties to genome-wide predictions
journal, March 2014

  • Shlyueva, Daria; Stampfel, Gerald; Stark, Alexander
  • Nature Reviews Genetics, Vol. 15, Issue 4
  • DOI: 10.1038/nrg3682

A Fruitful Decade Using Synthetic Promoters in the Improvement of Transgenic Plants
journal, November 2019


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
  • DOI: 10.1038/nrg3163

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
  • DOI: 10.1093/nar/gkaa682

The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


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
  • DOI: 10.1016/j.bbagrm.2013.10.005

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
  • DOI: 10.1038/7036

Synthetic Switches and Regulatory Circuits in Plants
journal, January 2019

  • Andres, Jennifer; Blomeier, Tim; Zurbriggen, Matias D.
  • Plant Physiology, Vol. 179, Issue 3
  • DOI: 10.1104/pp.18.01362

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
  • DOI: 10.1093/mp/sst146

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
  • DOI: 10.1104/pp.17.01462

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
  • DOI: 10.1111/tpj.13520

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
  • DOI: 10.1021/acssynbio.2c00147

Strength comparison between cold-inducible promoters of Arabidopsis cor15a and cor15b genes in potato and tobacco
journal, October 2013


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
  • DOI: 10.1093/pcp/pcu134

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
  • DOI: 10.3389/fpls.2020.00245

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
  • DOI: 10.1105/tpc.20.00155

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
  • DOI: 10.3390/ijms19071945

Transcript elongation factors: shaping transcriptomes after transcript initiation
journal, November 2014


Determinants of enhancer and promoter activities of regulatory elements
journal, October 2019


Plant synthetic biology
journal, May 2015


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
  • DOI: 10.1111/pbi.13510

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
  • DOI: 10.1038/nprot.2006.286

Synthetic promoter designs enabled by a comprehensive analysis of plant core promoters
journal, June 2021


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
  • DOI: 10.1111/pbi.13550

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
  • DOI: 10.1038/nature12787

Design of orthogonal regulatory systems for modulating gene expression in plants
journal, May 2020


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
  • DOI: 10.3389/fpls.2022.873480

Innovation in plant-based transient protein expression for infectious disease prevention and preparedness
journal, February 2020


Synthetic promoters in planta
journal, August 2015


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
  • DOI: 10.1038/nbt.3754

Plant synthetic promoters and transcription factors
journal, February 2016


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
  • DOI: 10.1111/pbi.12989

Abiotic stress responses in plants
journal, September 2021


Model-driven generation of artificial yeast promoters
journal, April 2020


Systematic interrogation of human promoters
journal, January 2019

  • Weingarten-Gabbay, Shira; Nir, Ronit; Lubliner, Shai
  • Genome Research, Vol. 29, Issue 2
  • DOI: 10.1101/gr.236075.118

Systematic Localization of Common Disease-Associated Variation in Regulatory DNA
journal, September 2012