Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield

Friedland, N.; Negi, S.; Vinogradova-Shah, T.; Wu, G.; Ma, L.; Flynn, S.; Kumssa, T.; Lee, C. -H.; Sayre, R. T.

doi:10.1038/s41598-019-49545-8

Title: Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield

Abstract

Photosynthetic electron transport rates in higher plants and green algae are light-saturated at approximately one quarter of full sunlight intensity. This is due to the large optical cross section of plant light harvesting antenna complexes which capture photons at a rate nearly 10-fold faster than the rate-limiting step in electron transport. As a result, 75% of the light captured at full sunlight intensities is reradiated as heat or fluorescence. Previously, it has been demonstrated that reductions in the optical cross-section of the light-harvesting antenna can lead to substantial improvements in algal photosynthetic rates and biomass yield. By surveying a range of light harvesting antenna sizes achieved by reduction in chlorophyll b levels, we have determined that there is an optimal light-harvesting antenna size that results in the greatest whole plant photosynthetic performance. We also uncover a sharp transition point where further reductions or increases in antenna size reduce photosynthetic efficiency, tolerance to light stress, and impact thylakoid membrane architecture. Plants with optimized antenna sizes are shown to perform well not only in controlled greenhouse conditions, but also in the field achieving a 40% increase in biomass yield.

Authors:

Friedland, N. ^[1]; Negi, S. ^[1]; Vinogradova-Shah, T. ^[2]; Wu, G. ^[3]; Ma, L. ^[3]; Flynn, S. ^[1]; Kumssa, T. ^[4]; Lee, C. -H. ^[3];

^[2]

New Mexico Consortium, Los Alamos, NM (United States)
New Mexico Consortium, Los Alamos, NM (United States); Pebble Labs, Los Alamos, NM (United States)
New Mexico Consortium, Los Alamos, NM (United States); Pusan National Univ., Busan (Korea, Republic of)
Univ. of Nebraska, Lincoln, NE (United States)

Publication Date:: Tue Sep 10 00:00:00 EDT 2019

Research Org.:: Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Org.:: USDOE Advanced Research Projects Agency - Energy (ARPA-E)

OSTI Identifier:: 1613560

Grant/Contract Number:: AR0000202

Resource Type:: Accepted Manuscript

Journal Name:: Scientific Reports

Additional Journal Information:: Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2045-2322

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 09 BIOMASS FUELS; Science & Technology

Citation Formats


                    Friedland, N., Negi, S., Vinogradova-Shah, T., Wu, G., Ma, L., Flynn, S., Kumssa, T., Lee, C. -H., and Sayre, R. T. Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield.  United States: N. p., 2019. 
Web.  doi:10.1038/s41598-019-49545-8.

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                    Friedland, N., Negi, S., Vinogradova-Shah, T., Wu, G., Ma, L., Flynn, S., Kumssa, T., Lee, C. -H., & Sayre, R. T. Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield.  United States.  https://doi.org/10.1038/s41598-019-49545-8

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                    Friedland, N., Negi, S., Vinogradova-Shah, T., Wu, G., Ma, L., Flynn, S., Kumssa, T., Lee, C. -H., and Sayre, R. T. Tue .  
"Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield".  United States.  https://doi.org/10.1038/s41598-019-49545-8.  https://www.osti.gov/servlets/purl/1613560.

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@article{osti_1613560,

  title        = {Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield},

  author       = {Friedland, N. and Negi, S. and Vinogradova-Shah, T. and Wu, G. and Ma, L. and Flynn, S. and Kumssa, T. and Lee, C. -H. and Sayre, R. T.},

  abstractNote = {Photosynthetic electron transport rates in higher plants and green algae are light-saturated at approximately one quarter of full sunlight intensity. This is due to the large optical cross section of plant light harvesting antenna complexes which capture photons at a rate nearly 10-fold faster than the rate-limiting step in electron transport. As a result, 75% of the light captured at full sunlight intensities is reradiated as heat or fluorescence. Previously, it has been demonstrated that reductions in the optical cross-section of the light-harvesting antenna can lead to substantial improvements in algal photosynthetic rates and biomass yield. By surveying a range of light harvesting antenna sizes achieved by reduction in chlorophyll b levels, we have determined that there is an optimal light-harvesting antenna size that results in the greatest whole plant photosynthetic performance. We also uncover a sharp transition point where further reductions or increases in antenna size reduce photosynthetic efficiency, tolerance to light stress, and impact thylakoid membrane architecture. Plants with optimized antenna sizes are shown to perform well not only in controlled greenhouse conditions, but also in the field achieving a 40% increase in biomass yield.},

  doi          = {10.1038/s41598-019-49545-8},

  journal      = {Scientific Reports},

  number       = 1,

  volume       = 9,

  place        = {United States},

  year         = {Tue Sep 10 00:00:00 EDT 2019},

  month        = {Tue Sep 10 00:00:00 EDT 2019}

}

Copy to clipboard

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Works referenced in this record:

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Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3
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Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii
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Beckmann, J.; Lehr, F.; Finazzi, G.
Journal of Biotechnology, Vol. 142, Issue 1
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Zhu, Xin-Guang; Song, Qingfeng; Ort, Donald R.
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Redesigning photosynthesis to sustainably meet global food and bioenergy demand
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Ort, Donald R.; Merchant, Sabeeha S.; Alric, Jean
Proceedings of the National Academy of Sciences, Vol. 112, Issue 28
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Tanaka, A.; Ito, H.; Tanaka, R.
Proceedings of the National Academy of Sciences, Vol. 95, Issue 21
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Optimizing Antenna Size to Maximize Photosynthetic Efficiency
journal, November 2010

Ort, Donald R.; Zhu, Xinguang; Melis, Anastasios
Plant Physiology, Vol. 155, Issue 1
DOI: 10.1104/pp.110.165886

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene
journal, November 2011

Kirst, Henning; García-Cerdán, Jose Gines; Zurbriggen, Andreas
Plant Physiology, Vol. 158, Issue 2
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COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949

Arnon, Daniel I.
Plant Physiology, Vol. 24, Issue 1
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Chloroplast Composition and Structure Differences in a Soybean Mutant
journal, November 1970

Keck, Robert W.; Dilley, Richard A.; Allen, C. Freeman
Plant Physiology, Vol. 46, Issue 5
DOI: 10.1104/pp.46.5.692

Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts
journal, November 2006

Kovács, László; Damkjær, Jakob; Kereïche, Sami
The Plant Cell, Vol. 18, Issue 11
DOI: 10.1105/tpc.106.045641

Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis
journal, April 2008

de Bianchi, Silvia; Dall'Osto, Luca; Tognon, Giuseppe
The Plant Cell, Vol. 20, Issue 4
DOI: 10.1105/tpc.107.055749

Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion
journal, November 2007

Mussgnug, Jan H.; Thomas-Hall, Skye; Rupprecht, Jens
Plant Biotechnology Journal, Vol. 5, Issue 6
DOI: 10.1111/j.1467-7652.2007.00285.x

Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane
journal, November 2017

Rantala, Marjaana; Tikkanen, Mikko; Aro, Eva-Mari
The Plant Journal, Vol. 92, Issue 5
DOI: 10.1111/tpj.13732

Structure and Membrane Organization of Photosystem ii in Green Plants
journal, June 1997

Hankamer, Ben; Barber, James; Boekema, Egbert J.
Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 48, Issue 1
DOI: 10.1146/annurev.arplant.48.1.641

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production
journal, January 2013

Subramanian, Sowmya; Barry, Amanda N.; Pieris, Shayani
Biotechnology for Biofuels, Vol. 6, Issue 1
DOI: 10.1186/1754-6834-6-150

Coexistence between fluid and crystalline phases of proteins in photosynthetic membranes
text, January 2013

Schneider, Anna R.; Geissler, Phillip L.
arXiv
DOI: 10.48550/arxiv.1302.6323

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Title: Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield

Abstract

Citation Formats

Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions Independent of Binding to PSII Antennae journal, October 2007

Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts journal, May 2007

COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS journal, January 1949

Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii journal, June 2009

Coexistence of Fluid and Crystalline Phases of Proteins in Photosynthetic Membranes journal, September 2013

The chloroplast signal recognition particle (CpSRP) pathway as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity journal, January 2014

Optimizing Antenna Size to Maximize Photosynthetic Efficiency journal, November 2010

Optimization of photosynthetic light energy utilization by microalgae journal, October 2012

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene journal, November 2011

Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts journal, November 2006

Characterization of the Arabidopsis thaliana Mutant pcb2 which Accumulates Divinyl Chlorophylls journal, March 2005

Characterization of Canopy Photosynthesis of Chlorophyll‐Deficient Soybean Isolines journal, July 1989

High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana journal, March 2013

Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes journal, December 1999

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production journal, January 2013

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal, December 1998

Supramolecular organization of thylakoid membrane proteins in green plants journal, January 2005

Characterization of PSII–LHCII supercomplexes isolated from pea thylakoid membrane by one-step treatment with α- and β-dodecyl- d -maltoside journal, December 2012

Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy journal, August 1989

Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane journal, November 2017

Chloroplast Composition and Structure Differences in a Soybean Mutant journal, November 1970

Supramolecular organization of photosystem II in green plants journal, January 2012

Redesigning photosynthesis to sustainably meet global food and bioenergy demand journal, June 2015

Elements of a dynamic systems model of canopy photosynthesis journal, June 2012

Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis journal, April 2008

Structure and Membrane Organization of Photosystem ii in Green Plants journal, June 1997

Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a journal, October 1998

Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion journal, November 2007

Functional architecture of higher plant photosystem II supercomplexes journal, August 2009

Quality Control of PSII: Behavior of PSII in the Highly Crowded Grana Thylakoids Under Excessive Light journal, March 2014

Photosynthetic rate and chlorophyll fluorescence of barley exposed to simulated acid rain journal, April 2021

Co-incorporation of manure and inorganic fertilizer improves leaf physiological traits, rice production and soil functionality in a paddy field journal, May 2021

Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts journal, May 2007

Supramolecular organization of thylakoid membrane proteins in green plants journal, January 2005

Supramolecular organization of photosystem II in green plants journal, January 2012

High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana journal, March 2013

Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii journal, June 2009

Elements of a dynamic systems model of canopy photosynthesis journal, June 2012

Functional architecture of higher plant photosystem II supercomplexes journal, August 2009

The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure journal, April 2014

Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes journal, September 2011

Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes journal, December 1999

Redesigning photosynthesis to sustainably meet global food and bioenergy demand journal, June 2015

Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a journal, October 1998

Optimizing Antenna Size to Maximize Photosynthetic Efficiency journal, November 2010

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene journal, November 2011

COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS journal, January 1949

Chloroplast Composition and Structure Differences in a Soybean Mutant journal, November 1970

Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts journal, November 2006

Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis journal, April 2008

Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion journal, November 2007

Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane journal, November 2017

Structure and Membrane Organization of Photosystem ii in Green Plants journal, June 1997

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production journal, January 2013

Coexistence between fluid and crystalline phases of proteins in photosynthetic membranes text, January 2013

The Effect of Red & Blue Rich LEDs vs Fluorescent Light on Lollo Rosso Lettuce Morphology and Physiology journal, February 2021

Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions Independent of Binding to PSII Antennae
journal, October 2007

Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts
journal, May 2007

COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949

Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii
journal, June 2009

Coexistence of Fluid and Crystalline Phases of Proteins in Photosynthetic Membranes
journal, September 2013

The chloroplast signal recognition particle (CpSRP) pathway as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity
journal, January 2014

Optimizing Antenna Size to Maximize Photosynthetic Efficiency
journal, November 2010

Optimization of photosynthetic light energy utilization by microalgae
journal, October 2012

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene
journal, November 2011

Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts
journal, November 2006

Characterization of the Arabidopsis thaliana Mutant pcb2 which Accumulates Divinyl Chlorophylls
journal, March 2005

Characterization of Canopy Photosynthesis of Chlorophyll‐Deficient Soybean Isolines
journal, July 1989

High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana
journal, March 2013

Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes
journal, December 1999

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production
journal, January 2013

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

Supramolecular organization of thylakoid membrane proteins in green plants
journal, January 2005

Characterization of PSII–LHCII supercomplexes isolated from pea thylakoid membrane by one-step treatment with α- and β-dodecyl- d -maltoside
journal, December 2012

Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy
journal, August 1989

Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane
journal, November 2017

Chloroplast Composition and Structure Differences in a Soybean Mutant
journal, November 1970

Supramolecular organization of photosystem II in green plants
journal, January 2012

Redesigning photosynthesis to sustainably meet global food and bioenergy demand
journal, June 2015

Elements of a dynamic systems model of canopy photosynthesis
journal, June 2012

Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis
journal, April 2008

Structure and Membrane Organization of Photosystem ii in Green Plants
journal, June 1997

Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a
journal, October 1998

Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion
journal, November 2007

Functional architecture of higher plant photosystem II supercomplexes
journal, August 2009

Quality Control of PSII: Behavior of PSII in the Highly Crowded Grana Thylakoids Under Excessive Light
journal, March 2014

Photosynthetic rate and chlorophyll fluorescence of barley exposed to simulated acid rain
journal, April 2021

Co-incorporation of manure and inorganic fertilizer improves leaf physiological traits, rice production and soil functionality in a paddy field
journal, May 2021

Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts
journal, May 2007

Supramolecular organization of thylakoid membrane proteins in green plants
journal, January 2005

Supramolecular organization of photosystem II in green plants
journal, January 2012

High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana
journal, March 2013

Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii
journal, June 2009

Elements of a dynamic systems model of canopy photosynthesis
journal, June 2012

Functional architecture of higher plant photosystem II supercomplexes
journal, August 2009

The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure
journal, April 2014

Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes
journal, September 2011

Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes
journal, December 1999

Redesigning photosynthesis to sustainably meet global food and bioenergy demand
journal, June 2015

Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a
journal, October 1998

Optimizing Antenna Size to Maximize Photosynthetic Efficiency
journal, November 2010

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene
journal, November 2011

COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949

Chloroplast Composition and Structure Differences in a Soybean Mutant
journal, November 1970

Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts
journal, November 2006

Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis
journal, April 2008

Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion
journal, November 2007

Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane
journal, November 2017

Structure and Membrane Organization of Photosystem ii in Green Plants
journal, June 1997

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production
journal, January 2013

Coexistence between fluid and crystalline phases of proteins in photosynthetic membranes
text, January 2013

The Effect of Red & Blue Rich LEDs vs Fluorescent Light on Lollo Rosso Lettuce Morphology and Physiology
journal, February 2021