Please confirm you are human (Sign Up for free to never see this)
← Back to Search
Combining Genetic And Evolutionary Engineering To Establish C4 Metabolism In C3 Plants.
Y. Li, D. Heckmann, M. Lercher, V. Maurino
Published 2017 · Biology, Medicine
Save to my Library
Download PDFAnalyze on Scholarcy
To feed a world population projected to reach 9 billion people by 2050, the productivity of major crops must be increased by at least 50%. One potential route to boost the productivity of cereals is to equip them genetically with the 'supercharged' C4 type of photosynthesis; however, the necessary genetic modifications are not sufficiently understood for the corresponding genetic engineering programme. In this opinion paper, we discuss a strategy to solve this problem by developing a new paradigm for plant breeding. We propose combining the bioengineering of well-understood traits with subsequent evolutionary engineering, i.e. mutagenesis and artificial selection. An existing mathematical model of C3-C4 evolution is used to choose the most promising path towards this goal. Based on biomathematical simulations, we engineer Arabidopsis thaliana plants that express the central carbon-fixing enzyme Rubisco only in bundle sheath cells (Ru-BSC plants), the localization characteristic for C4 plants. This modification will initially be deleterious, forcing the Ru-BSC plants into a fitness valley from where previously inaccessible adaptive steps towards C4 photosynthesis become accessible through fitness-enhancing mutations. Mutagenized Ru-BSC plants are then screened for improved photosynthesis, and are expected to respond to imposed artificial selection pressures by evolving towards C4 anatomy and biochemistry.
This paper references
The Gene for the P-Subunit of Glycine Decarboxylase from the C4 Species Flaveria trinervia: Analysis of Transcriptional Control in Transgenic Flaveria bidentis (C4) and Arabidopsis (C3)1[W][OA]
S. Engelmann (2008)
The role of proteins in C(3) plants prior to their recruitment into the C(4) pathway.
Sylvain Aubry (2011)
Engineering photosynthesis in plants and synthetic microorganisms.
V. Maurino (2013)
The Yeast Environmental Stress Response Regulates Mutagenesis Induced by Proteotoxic Stress
E. Shor (2013)
A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame.
R. Sage (2016)
Supercharging rice photosynthesis to increase yield.
P. Mitchell (2006)
Malate decarboxylases: evolution and roles of NAD(P)-ME isoforms in species performing C(4) and C(3) photosynthesis.
Alexandra Maier (2011)
Isoleucine 309 acts as a C4 catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria
S. Whitney (2011)
Integrating C4 photosynthesis into C3 crops to increase yield potential.
Sarah Covshoff (2012)
2-Hydroxy Acids in Plant Metabolism
Veronica G. Maurino (2015)
Photorespiration: current status and approaches for metabolic engineering.
V. Maurino (2010)
Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape
Yonatan Savir (2010)
Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco1[W]
S. Whitney (2010)
The Development of C4 Rice: Current Progress and Future Challenges
S. von Caemmerer (2012)
Photorespiratory glycolate-glyoxylate metabolism.
Younès Dellero (2016)
Elucidating Rice Cell Metabolism under Flooding and Drought Stresses Using Flux-Based Modeling and Analysis1[C][W][OPEN]
M. Lakshmanan (2013)
Predicting C4 Photosynthesis Evolution: Modular, Individually Adaptive Steps on a Mount Fuji Fitness Landscape
David Heckmann (2013)
Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation
J. Ehleringer (1993)
The Path from C3 to C4 Photosynthesis1
U. Gowik (2010)
Lessons from Domestication: Targeting Cis-Regulatory Elements for Crop Improvement.
Gwen Swinnen (2016)
Biochemical models of leaf photosynthesis.
S. V. Caemmerer (2000)
The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
S. Ossowski (2010)
Manipulation of Rubisco: the amount, activity, function and regulation.
M. Parry (2003)
Tissue distribution of primary metabolism between epidermal, mesophyll and parenchymatous bundle sheath cells in barley leaves
O. Koroleva (2000)
Chapter 14 C 4 Decarboxylases: Different Solutions for the Same Biochemical Problem, the Provision of CO 2 to Rubisco in the Bundle Sheath Cells
M. F. Drincovich (2010)
The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria
J. Mallmann (2014)
Photorespiration and the evolution of C4 photosynthesis.
R. Sage (2012)
Evolution of C4 phosphoenolpyruvate carboxylase.
P. Svensson (2003)
Mutagenesis as a Tool in Plant Genetics, Functional Genomics, and Breeding
Per Sikora (2011)
cis-Regulatory Elements for Mesophyll-Specific Gene Expression in the C4 Plant Flaveria trinervia, the Promoter of the C4 Phosphoenolpyruvate Carboxylase Gene
U. Gowik (2004)
Cell specialization within the parenchymatous bundle sheath of barley
M. Williams (1989)
Ethylmethanesulfonate Saturation Mutagenesis in Arabidopsis to Determine Frequency of Herbicide Resistance
G. Jander (2003)
An mRNA Blueprint for C4 Photosynthesis Derived from Comparative Transcriptomics of Closely Related C3 and C4 Species1[W][OA]
A. Bräutigam (2010)
Prospects for increasing photosynthesis by overcoming the limitations of Rubisco
M. Parry (2007)
Reaping the Benefits: Science and the sustainable intensification of global agriculture
B. Davies (2009)
Naturally occurring genetic variation in Arabidopsis thaliana.
M. Koornneef (2004)
A novel RNA binding protein affects rbcL gene expression and is specific to bundle sheath chloroplasts in C4 plants
Shaun M. Bowman (2013)
Increasing Leaf Vein Density by Mutagenesis: Laying the Foundations for C4 Rice
Aryo B. Feldman (2014)
Adaptive laboratory evolution – principles and applications for biotechnology
Martin Dragosits (2013)
Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations.
Caifu Jiang (2014)
The Royal Society of London
G. Box (2013)
Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C4 pathway
Shanta Karki (2013)
The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana.
H. Takahashi (2000)
Improving photosynthetic efficiency for greater yield.
Xin-Guang Zhu (2010)
Estimation of the whole‐plant CO2 compensation point of tobacco (Nicotiana tabacum L.)
C. Campbell (2005)
An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells[OPEN]
Ben P. Williams (2016)
Carbon isotope discrimination as a diagnostic tool for C4 photosynthesis in C3-C4 intermediate species
Hugo Alonso-Cantabrana (2016)
Roles of the bundle sheath cells in leaves of C3 plants.
R. Leegood (2008)
Mutation as a Stress Response and the Regulation of Evolvability
R. Galhardo (2007)
Evolution of the C(4) photosynthetic mechanism: are there really three C(4) acid decarboxylation types?
R. Furbank (2011)
A faster Rubisco with potential to increase photosynthesis in crops
Myat T Lin (2014)
An integrated approach to characterize genetic interaction networks in yeast metabolism
Balázs Szappanos (2011)
Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves.
J. M. Pérez-Pérez (2002)
Regulation of DNA repair in hypoxic cancer cells
R. Bindra (2007)
Activation tagging in Arabidopsis.
D. Weigel (2000)
Whole organ, venation and epidermal cell morphological variations are correlated in the leaves of Arabidopsis mutants.
J. M. Pérez-Pérez (2011)
Adaptive laboratory evolution--harnessing the power of biology for metabolic engineering.
Vasiliy Portnoy (2011)
Imaging of photo-oxidative stress responses in leaves.
M. Fryer (2002)
Can perennial C4 grasses attain high efficiencies of radiant energy conversion in cool climates
C. V. Beale (1995)
Identity and Function of a Large Gene Network Underlying Mutagenic Repair of DNA Breaks
A. A. A. Al Mamun (2012)
Subunit control of Rubisco biosynthesis – a relic of an endosymbiotic past?
S. Rodermel (2004)
Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves.
E. Kinsman (1998)
This paper is referenced by
Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C 4 plants
Using energy-efficient synthetic biochemical pathways to bypass photorespiration.
V. Maurino (2019)
Improved water use efficiency and shorter life cycle of Nicotiana tabacum due to modification of guard and vascular companion cells
G. Müller (2018)
Developing C4 Rice for Higher Photosynthetic Efficiency and Environmental Stress Tolerance
Aisha Kamal (2020)
Engineering central metabolism – a grand challenge for plant biologists
Lee J. Sweetlove (2017)
Target genes for plant productivity improvement.
B. Nowicka (2019)
Synchronization of developmental, molecular and metabolic aspects of source–sink interactions
A. Fernie (2020)
Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C4 plants.
I. Turkan (2018)
Biochemical control systems for small molecule damage in plants
M. Hüdig (2018)
Functional Diversity of Photosynthesis, Plant-Species Diversity, and Habitat Diversity
U. Lüttge (2019)
Exploring natural variation of photosynthesis in a site-specific manner: evolution, progress, and prospects
P. Dehigaspitiya (2019)
Update: Improving the Efficiency of Photosynthetic Carbon Reactions1[OPEN]
A. Weber (2019)
C4 photosynthesis: 50 years of discovery and innovation
S. von Caemmerer (2017)