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Title: Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes

Abstract

In C 3 plants, the carbon fixation step catalyzed by ribulose -1,5-bisphosphate carboxylase/oxygenase (Rubisco) represents a major rate-limiting step due to the competing oxygenation reaction, which leads to the energy-intensive photorespiration and lowers the overall photosynthetic efficiency. Hence, there is great biotechnological interest in replacing the Rubisco in C 3 crops with a more efficient enzyme. The Rubisco enzymes from red algae are among the most attractive choices due to their remarkable preference for carboxylation over oxygenation reaction. However, the biogenesis of Rubisco is extremely complex. The Rubisco enzymes in plants, algae, and cyanobacteria are made up of eight large and eight small subunits. The folding of the large subunits and the assembly of the large subunits with the small subunits to form a functional holoenzyme require specific chaperonin complexes and assembly factors. As a result, previous success in expressing foreign Rubisco in plants has been limited to Rubisco large subunits from closely related plant species and simpler bacterial enzymes. In our previous work, we successfully replaced the Rubisco in tobacco with a cyanobacterial enzyme, which was able to support the phototrophic growth of the transgenic plants. In this work, we used the same approach to express the Rubisco subunitsmore » from the red alga Griffithsia monilis in tobacco chloroplasts in the absence of the tobacco Rubisco large subunit. Although the red algal Rubisco genes are being transcribed in tobacco chloroplasts, the transgenic plants lack functional Rubisco and can only grow in a medium containing sucrose. Our results suggest that co-expression of compatible chaperones will be necessary for successful assembly of red algal Rubisco in plants.« less

Authors:
 [1];  [1]
  1. Department of Molecular Biology and Genetics, Cornell University, Ithaca NY USA
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1423168
Alternate Identifier(s):
OSTI ID: 1423170; OSTI ID: 1623583
Grant/Contract Number:  
SC0014339
Resource Type:
Journal Article: Published Article
Journal Name:
Plant Direct
Additional Journal Information:
Journal Name: Plant Direct Journal Volume: 2 Journal Issue: 2; Journal ID: ISSN 2475-4455
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
United Kingdom
Language:
English
Subject:
Plant Sciences

Citation Formats

Lin, Myat T., and Hanson, Maureen R. Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes. United Kingdom: N. p., 2018. Web. doi:10.1002/pld3.45.
Lin, Myat T., & Hanson, Maureen R. Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes. United Kingdom. https://doi.org/10.1002/pld3.45
Lin, Myat T., and Hanson, Maureen R. Wed . "Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes". United Kingdom. https://doi.org/10.1002/pld3.45.
@article{osti_1423168,
title = {Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes},
author = {Lin, Myat T. and Hanson, Maureen R.},
abstractNote = {In C3 plants, the carbon fixation step catalyzed by ribulose -1,5-bisphosphate carboxylase/oxygenase (Rubisco) represents a major rate-limiting step due to the competing oxygenation reaction, which leads to the energy-intensive photorespiration and lowers the overall photosynthetic efficiency. Hence, there is great biotechnological interest in replacing the Rubisco in C3 crops with a more efficient enzyme. The Rubisco enzymes from red algae are among the most attractive choices due to their remarkable preference for carboxylation over oxygenation reaction. However, the biogenesis of Rubisco is extremely complex. The Rubisco enzymes in plants, algae, and cyanobacteria are made up of eight large and eight small subunits. The folding of the large subunits and the assembly of the large subunits with the small subunits to form a functional holoenzyme require specific chaperonin complexes and assembly factors. As a result, previous success in expressing foreign Rubisco in plants has been limited to Rubisco large subunits from closely related plant species and simpler bacterial enzymes. In our previous work, we successfully replaced the Rubisco in tobacco with a cyanobacterial enzyme, which was able to support the phototrophic growth of the transgenic plants. In this work, we used the same approach to express the Rubisco subunits from the red alga Griffithsia monilis in tobacco chloroplasts in the absence of the tobacco Rubisco large subunit. Although the red algal Rubisco genes are being transcribed in tobacco chloroplasts, the transgenic plants lack functional Rubisco and can only grow in a medium containing sucrose. Our results suggest that co-expression of compatible chaperones will be necessary for successful assembly of red algal Rubisco in plants.},
doi = {10.1002/pld3.45},
url = {https://www.osti.gov/biblio/1423168}, journal = {Plant Direct},
issn = {2475-4455},
number = 2,
volume = 2,
place = {United Kingdom},
year = {2018},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1002/pld3.45

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

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Works referenced in this record:

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journal, June 2007


Chaperonin Cofactors, Cpn10 and Cpn20, of Green Algae and Plants Function as Hetero-oligomeric Ring Complexes
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A protein with an inactive pterin-4a-carbinolamine dehydratase domain is required for Rubisco biogenesis in plants
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Redesigning photosynthesis to sustainably meet global food and bioenergy demand
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Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants
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Evolving Methanococcoides burtonii archaeal Rubisco for improved photosynthesis and plant growth
journal, March 2016


Structural insight into the cooperation of chloroplast chaperonin subunits
journal, April 2016


Coupled chaperone action in folding and assembly of hexadecameric Rubisco
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BUNDLE SHEATH DEFECTIVE2, a Novel Protein Required for Post-Translational Regulation of the rbcL Gene of Maize
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Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape
journal, February 2010


Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms
journal, April 2016


    Works referencing / citing this record:

    Field-grown tobacco plants maintain robust growth while accumulating large quantities of a bacterial cellulase in chloroplasts
    journal, July 2019


    Directed Evolution of an Improved Rubisco; In Vitro Analyses to Decipher Fact from Fiction
    journal, October 2019