Generation, analysis, and transformation of macro-chloroplast Potato (Solanum tuberosum) lines for chloroplast biotechnology
Abstract
Abstract Chloroplast biotechnology is a route for novel crop metabolic engineering. The potential bio-confinement of transgenes, the high protein expression and the possibility to organize genes into operons represent considerable advantages that make chloroplasts valuable targets in agricultural biotechnology. In the last 3 decades, chloroplast genomes from a few economically important crops have been successfully transformed. The main bottlenecks that prevent efficient transformation in a greater number of crops include the dearth of proven selectable marker gene-selection combinations and tissue culture methods for efficient regeneration of transplastomic plants. The prospects of increasing organelle size are attractive from several perspectives, including an increase in the surface area of potential targets. As a proof-of-concept, we generated Solanum tuberosum (potato) macro-chloroplast lines overexpressing the tubulin-like GTPase protein gene FtsZ1 from Arabidopsis thaliana . Macro-chloroplast lines exhibited delayed growth at anthesis; however, at the time of harvest there was no significant difference in height between macro-chloroplast and wild-type lines. Macro-chloroplasts were successfully transformed by biolistic DNA-delivery and efficiently regenerated into homoplasmic transplastomic lines. We also demonstrated that macro-chloroplasts accumulate the same amount of heterologous protein than wild-type organelles, confirming efficient usage in plastid engineering. Advantages and limitations of using enlarge compartments in chloroplast biotechnologymore »
- Publication Date:
- Sponsoring Org.:
- USDOE Advanced Research Projects Agency - Energy (ARPA-E)
- OSTI Identifier:
- 1730964
- Grant/Contract Number:
- AR000660
- Resource Type:
- Published Article
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Name: Scientific Reports Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Occhialini, Alessandro, Pfotenhauer, Alexander C., Frazier, Taylor P., Li, Li, Harbison, Stacee A., Lail, Andrew J., Mebane, Zachary, Piatek, Agnieszka A., Rigoulot, Stephen B., Daniell, Henry, Stewart, Jr, C. Neal, and Lenaghan, Scott C. Generation, analysis, and transformation of macro-chloroplast Potato (Solanum tuberosum) lines for chloroplast biotechnology. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41598-020-78237-x.
Occhialini, Alessandro, Pfotenhauer, Alexander C., Frazier, Taylor P., Li, Li, Harbison, Stacee A., Lail, Andrew J., Mebane, Zachary, Piatek, Agnieszka A., Rigoulot, Stephen B., Daniell, Henry, Stewart, Jr, C. Neal, & Lenaghan, Scott C. Generation, analysis, and transformation of macro-chloroplast Potato (Solanum tuberosum) lines for chloroplast biotechnology. United Kingdom. https://doi.org/10.1038/s41598-020-78237-x
Occhialini, Alessandro, Pfotenhauer, Alexander C., Frazier, Taylor P., Li, Li, Harbison, Stacee A., Lail, Andrew J., Mebane, Zachary, Piatek, Agnieszka A., Rigoulot, Stephen B., Daniell, Henry, Stewart, Jr, C. Neal, and Lenaghan, Scott C. Thu .
"Generation, analysis, and transformation of macro-chloroplast Potato (Solanum tuberosum) lines for chloroplast biotechnology". United Kingdom. https://doi.org/10.1038/s41598-020-78237-x.
@article{osti_1730964,
title = {Generation, analysis, and transformation of macro-chloroplast Potato (Solanum tuberosum) lines for chloroplast biotechnology},
author = {Occhialini, Alessandro and Pfotenhauer, Alexander C. and Frazier, Taylor P. and Li, Li and Harbison, Stacee A. and Lail, Andrew J. and Mebane, Zachary and Piatek, Agnieszka A. and Rigoulot, Stephen B. and Daniell, Henry and Stewart, Jr, C. Neal and Lenaghan, Scott C.},
abstractNote = {Abstract Chloroplast biotechnology is a route for novel crop metabolic engineering. The potential bio-confinement of transgenes, the high protein expression and the possibility to organize genes into operons represent considerable advantages that make chloroplasts valuable targets in agricultural biotechnology. In the last 3 decades, chloroplast genomes from a few economically important crops have been successfully transformed. The main bottlenecks that prevent efficient transformation in a greater number of crops include the dearth of proven selectable marker gene-selection combinations and tissue culture methods for efficient regeneration of transplastomic plants. The prospects of increasing organelle size are attractive from several perspectives, including an increase in the surface area of potential targets. As a proof-of-concept, we generated Solanum tuberosum (potato) macro-chloroplast lines overexpressing the tubulin-like GTPase protein gene FtsZ1 from Arabidopsis thaliana . Macro-chloroplast lines exhibited delayed growth at anthesis; however, at the time of harvest there was no significant difference in height between macro-chloroplast and wild-type lines. Macro-chloroplasts were successfully transformed by biolistic DNA-delivery and efficiently regenerated into homoplasmic transplastomic lines. We also demonstrated that macro-chloroplasts accumulate the same amount of heterologous protein than wild-type organelles, confirming efficient usage in plastid engineering. Advantages and limitations of using enlarge compartments in chloroplast biotechnology are discussed.},
doi = {10.1038/s41598-020-78237-x},
journal = {Scientific Reports},
number = 1,
volume = 10,
place = {United Kingdom},
year = {2020},
month = {12}
}
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Works referenced in this record:
High-Throughput Genotyping of Green Algal Mutants Reveals Random Distribution of Mutagenic Insertion Sites and Endonucleolytic Cleavage of Transforming DNA
journal, April 2014
- Zhang, Ru; Patena, Weronika; Armbruster, Ute
- The Plant Cell, Vol. 26, Issue 4
Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses
journal, January 2014
- Chen, Peng-Jen; Senthilkumar, Rajendran; Jane, Wann-Neng
- Plant Biotechnology Journal, Vol. 12, Issue 4
High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene.
journal, February 1993
- Svab, Z.; Maliga, P.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 3
Validation of leaf enzymes in the detergent and textile industries: launching of a new platform technology
journal, February 2019
- Kumari, Uma; Singh, Rahul; Ray, Tui
- Plant Biotechnology Journal, Vol. 17, Issue 6
Non-photosynthetic plastids as hosts for metabolic engineering
journal, February 2018
- Mellor, Silas Busck; Behrendorff, James B. Y. H.; Nielsen, Agnieszka Zygadlo
- Essays in Biochemistry, Vol. 62, Issue 1
Single Walled Carbon Nanotubes Exhibit Dual-Phase Regulation to Exposed Arabidopsis Mesophyll Cells
journal, September 2010
- Yuan, Hengguang; Hu, Shanglian; Huang, Peng
- Nanoscale Research Letters
MoChlo: A Versatile, Modular Cloning Toolbox for Chloroplast Biotechnology
journal, January 2019
- Occhialini, Alessandro; Piatek, Agnieszka A.; Pfotenhauer, Alexander C.
- Plant Physiology, Vol. 179, Issue 3
Release of Hormones from Conjugates: Chloroplast Expression of β-Glucosidase Results in Elevated Phytohormone Levels Associated with Significant Increase in Biomass and Protection from Aphids or Whiteflies Conferred by Sucrose Esters
journal, November 2010
- Jin, Shuangxia; Kanagaraj, Anderson; Verma, Dheeraj
- Plant Physiology, Vol. 155, Issue 1
Stable Plastid Transformation in PEG-treated Protoplasts of Nicotiana tabacum
journal, January 1993
- Golds, Timothy; Maliga, Pal; Koop, Hans-Ulrich
- Nature Biotechnology, Vol. 11, Issue 1
Ftsz Ring Formation at the Chloroplast Division Site in Plants
journal, April 2001
- Vitha, Stanislav; McAndrew, Rosemary S.; Osteryoung, Katherine W.
- The Journal of Cell Biology, Vol. 153, Issue 1
Visualization of an FtsZ Ring in Chloroplasts of Lilium longiflorum Leaves
journal, June 2001
- Mori, Toshiyuki; Kuroiwa, Haruko; Takahara, Manabu
- Plant and Cell Physiology, Vol. 42, Issue 6
Low cost industrial production of coagulation factor IX bioencapsulated in lettuce cells for oral tolerance induction in hemophilia B
journal, November 2015
- Su, Jin; Zhu, Liqing; Sherman, Alexandra
- Biomaterials, Vol. 70
Field production and functional evaluation of chloroplast-derived interferon-?2b
journal, July 2007
- Arlen, Philip A.; Falconer, Regina; Cherukumilli, Sri
- Plant Biotechnology Journal, Vol. 5, Issue 4
Growth retardation of plants transformed by overexpression of NtFtsZ1-2 in Tobacco
journal, June 2002
- Jeong, Won Joong; Jeong, Suk Won; Min, Sung Ran
- Journal of Plant Biology, Vol. 45, Issue 2
Plastid Biotechnology: Food, Fuel, and Medicine for the 21st Century
journal, January 2011
- Maliga, Pal; Bock, Ralph
- Plant Physiology, Vol. 155, Issue 4
β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts
journal, June 2014
- Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
- The Plant Journal, Vol. 79, Issue 1
A new synthetic biology approach allows transfer of an entire metabolic pathway from a medicinal plant to a biomass crop
journal, June 2016
- Fuentes, Paulina; Zhou, Fei; Erban, Alexander
- eLife, Vol. 5
Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial ftsZ
journal, December 1998
- Osteryoung, Katherine W.; Stokes, Kevin D.; Rutherford, Stephen M.
- The Plant Cell, Vol. 10, Issue 12
The Engineered Chloroplast Genome Just Got Smarter
journal, October 2015
- Jin, Shuangxia; Daniell, Henry
- Trends in Plant Science, Vol. 20, Issue 10
The plastid genome as a chassis for synthetic biology-enabled metabolic engineering: players in gene expression
journal, July 2018
- Schindel, Heidi S.; Piatek, Agnieszka A.; Stewart, C. Neal
- Plant Cell Reports, Vol. 37, Issue 10
Stable plastid transformation of rice, a monocot cereal crop
journal, September 2018
- Wang, Yunpeng; Wei, Zhengyi; Xing, Shaochen
- Biochemical and Biophysical Research Communications, Vol. 503, Issue 4
A faster Rubisco with potential to increase photosynthesis in crops
journal, September 2014
- Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
- Nature, Vol. 513, Issue 7519
Arabidopsis FtsZ2-1 and FtsZ2-2 Are Functionally Redundant, But FtsZ-Based Plastid Division Is Not Essential for Chloroplast Partitioning or Plant Growth and Development
journal, November 2009
- Schmitz, Aaron J.; Glynn, Jonathan M.; Olson, Bradley J. S. C.
- Molecular Plant, Vol. 2, Issue 6
A Large Population of Small Chloroplasts in Tobacco Leaf Cells Allows More Effective Chloroplast Movement Than a Few Enlarged Chloroplasts
journal, April 2002
- Jeong, Won Joong; Park, Youn-Il; Suh, KyeHong
- Plant Physiology, Vol. 129, Issue 1
Primer3—new capabilities and interfaces
journal, June 2012
- Untergasser, Andreas; Cutcutache, Ioana; Koressaar, Triinu
- Nucleic Acids Research, Vol. 40, Issue 15
Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit
journal, September 2001
- Ruf, Stephanie; Hermann, Marita; Berger, Irving J.
- Nature Biotechnology, Vol. 19, Issue 9
Expression of Brassica oleracea FtsZ1-1 and MinD alters chloroplast division in Nicotiana tabacum generating macro- and mini-chloroplasts
journal, December 2011
- Chikkala, Veera R. N.; Nugent, Gregory D.; Stalker, David M.
- Plant Cell Reports, Vol. 31, Issue 5
Plant cell-made protein antigens for induction of Oral tolerance
journal, November 2019
- Daniell, Henry; Kulis, Michael; Herzog, Roland W.
- Biotechnology Advances, Vol. 37, Issue 7
Colocalization of Plastid Division Proteins in the Chloroplast Stromal Compartment Establishes a New Functional Relationship between FtsZ1 and FtsZ2 in Higher Plants
journal, December 2001
- McAndrew, Rosemary S.; Froehlich, John E.; Vitha, Stanislav
- Plant Physiology, Vol. 127, Issue 4
Transgene containment by maternal inheritance: Effective or elusive?
journal, April 2007
- Daniell, H.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 17
A galinstan expansion femtosyringe for microinjection of eukaryotic organelles and prokaryotes
journal, September 1999
- Knoblauch, Michael; Hibberd, Julian M.; Gray, John C.
- Nature Biotechnology, Vol. 17, Issue 9
Cold chain and virus‐free oral polio booster vaccine made in lettuce chloroplasts confers protection against all three poliovirus serotypes
journal, January 2019
- Daniell, Henry; Rai, Vineeta; Xiao, Yuhong
- Plant Biotechnology Journal, Vol. 17, Issue 7
Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons
journal, February 2013
- Lu, Y.; Rijzaani, H.; Karcher, D.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 8
High-efficiency generation of fertile transplastomic Arabidopsis plants
journal, February 2019
- Ruf, Stephanie; Forner, Joachim; Hasse, Claudia
- Nature Plants, Vol. 5, Issue 3
Introduction and expression of foreign DNA in isolated spinach chloroplasts by electroporation
journal, October 1996
- To, Kin-Ying; Cheng, Ming-Chih; Chen, Long-Fang Oliver
- The Plant Journal, Vol. 10, Issue 4
Enhancement of Chloroplast Transformation Frequency by Using Mesophyll Cells Containing a Few Enlarged Chloroplasts from Nuclear Transformed Plants in Tobacco [적은 수의 거대 엽록체를 가진 핵 형질전환 식물체를 이용한 담배 엽록체 형질전환 빈도 제고]
journal, September 2007
- Jeong, Won-Joong; Min, Sung-Ran; Liu, Jang-R.
- Journal of Plant Biotechnology, Vol. 34, Issue 3
Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers
journal, February 2019
- Kwak, Seon-Yeong; Lew, Tedrick Thomas Salim; Sweeney, Connor J.
- Nature Nanotechnology, Vol. 14, Issue 5
Stable transformation of plastids in higher plants.
journal, November 1990
- Svab, Z.; Hajdukiewicz, P.; Maliga, P.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 21
Manipulation of starch granule size distribution in potato tubers by modulation of plastid division
journal, January 2006
- Pater, Sylvia; Caspers, Martien; Kottenhagen, Marijke
- Plant Biotechnology Journal, Vol. 4, Issue 1
Genome-Wide Analysis of Plastid Gene Expression in Potato Leaf Chloroplasts and Tuber Amyloplasts: Transcriptional and Posttranscriptional Control
journal, June 2009
- Valkov, Vladimir T.; Scotti, Nunzia; Kahlau, Sabine
- Plant Physiology, Vol. 150, Issue 4
Generation of homoplasmic plastid transformants of a commercial cultivar of potato (Solanum tuberosum L.)
journal, June 2005
- Nguyen, Thanh Thi; Nugent, Gregory; Cardi, Teodoro
- Plant Science, Vol. 168, Issue 6
Release of Proteins from Intact Chloroplasts Induced by Reactive Oxygen Species during Biotic and Abiotic Stress
journal, June 2013
- Kwon, Kwang-Chul; Verma, Dheeraj; Jin, Shuangxia
- PLoS ONE, Vol. 8, Issue 6
Transformation of Agrobacterium Using the Freeze-Thaw Method
journal, December 2006
- Weigel, D.; Glazebrook, J.
- Cold Spring Harbor Protocols, Vol. 2006, Issue 30
Participation of Leaky Ribosome Scanning in Protein Dual Targeting by Alternative Translation Initiation in Higher Plants
journal, January 2009
- Wamboldt, Yashitola; Mohammed, Saleem; Elowsky, Christian
- The Plant Cell, Vol. 21, Issue 1
Engineering Plastid Genomes: Methods, Tools, and Applications in Basic Research and Biotechnology
journal, April 2015
- Bock, Ralph
- Annual Review of Plant Biology, Vol. 66, Issue 1
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
Strategies for metabolic pathway engineering with multiple transgenes
journal, March 2013
- Bock, Ralph
- Plant Molecular Biology, Vol. 83, Issue 1-2
Engineered RNA-binding protein for transgene activation in non-green plastids
journal, April 2019
- Yu, Qiguo; Barkan, Alice; Maliga, Pal
- Nature Plants, Vol. 5, Issue 5
Direct cell to cell transfer of organelles by microinjection
journal, January 1992
- Verhoeven, HarrieA.; Blaas, Jan
- Plant Cell Reports, Vol. 10, Issue 12
Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome: Metabolic engineering in transplastomic tomatoes
journal, December 2006
- Wurbs, David; Ruf, Stephanie; Bock, Ralph
- The Plant Journal, Vol. 49, Issue 2
Investigational new drug enabling angiotensin oral-delivery studies to attenuate pulmonary hypertension
journal, March 2020
- Daniell, Henry; Mangu, Venkata; Yakubov, Bakhtiyor
- Biomaterials, Vol. 233
Division and Dynamic Morphology of Plastids
journal, April 2014
- Osteryoung, Katherine W.; Pyke, Kevin A.
- Annual Review of Plant Biology, Vol. 65, Issue 1
A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism
journal, February 2013
- Chronis, Demosthenis; Chen, Shiyan; Lu, Shunwen
- The Plant Journal, Vol. 74, Issue 2
Phenomics: the next challenge
journal, November 2010
- Houle, David; Govindaraju, Diddahally R.; Omholt, Stig
- Nature Reviews Genetics, Vol. 11, Issue 12
The Molecular Machinery of Chloroplast Division
journal, October 2017
- Chen, Cheng; MacCready, Joshua S.; Ducat, Daniel C.
- Plant Physiology, Vol. 176, Issue 1
Chloroplast Division and Morphology Are Differentially Affected by Overexpression of FtsZ1 and FtsZ2 Genes in Arabidopsis
journal, December 2000
- Stokes, Kevin D.; McAndrew, Rosemary S.; Figueroa, Rubi
- Plant Physiology, Vol. 124, Issue 4
Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO 2
journal, December 2015
- Occhialini, Alessandro; Lin, Myat T.; Andralojc, P. John
- The Plant Journal, Vol. 85, Issue 1
Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker
journal, July 1999
- Sidorov, Vladimir A.; Kasten, Daniel; Pang, Sheng-Zhi
- The Plant Journal, Vol. 19, Issue 2
Terpene metabolic engineering via nuclear or chloroplast genomes profoundly and globally impacts off-target pathways through metabolite signalling
journal, March 2016
- Pasoreck, Elise K.; Su, Jin; Silverman, Ian M.
- Plant Biotechnology Journal, Vol. 14, Issue 9
High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5′ and 3′ regulatory sequences
journal, May 2010
- Valkov, Vladimir T.; Gargano, Daniela; Manna, Carmela
- Transgenic Research, Vol. 20, Issue 1
Validation of leaf and microbial pectinases: commercial launching of a new platform technology
journal, February 2019
- Daniell, Henry; Ribeiro, Thuanne; Lin, Shina
- Plant Biotechnology Journal, Vol. 17, Issue 6
High-Frequency Transformation of Undeveloped Plastids in Tobacco Suspension Cells
journal, May 2004
- Langbecker, Camri L.; Ye, Guang-Ning; Broyles, Debra L.
- Plant Physiology, Vol. 135, Issue 1
Oral delivery of novel human IGF-1 bioencapsulated in lettuce cells promotes musculoskeletal cell proliferation, differentiation and diabetic fracture healing
journal, March 2020
- Park, J.; Yan, G.; Kwon, K. -C.
- Biomaterials, Vol. 233
Chloroplast Vector Systems for Biotechnology Applications
journal, December 2007
- Verma, Dheeraj; Daniell, Henry
- Plant Physiology, Vol. 145, Issue 4