Evolutionary transition from C3 to C4 photosynthesis and the route to C4 rice

AbstractCompared with C3 plants, C4 plants possess a mechanism to concentrate CO2 around the ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts of bundle sheath cells so that the carboxylation reaction work at a much more efficient rate, thereby substantially eliminate the oxygenation reaction and the resulting photorespiration. It is observed that C4 photosynthesis is more efficient than C3 photosynthesis under conditions of low atmospheric CO2, heat, drought and salinity, suggesting that these factors are the important drivers to promote C4 evolution. Although C4 evolution took over 66 times independently, it is hypothesized that it shared the following evolutionary trajectory: 1) gene duplication followed by neofunctionalization; 2) anatomical and ultrastructral changes of leaf architecture to improve the hydraulic systems; 3) establishment of two-celled photorespiratory pump; 4) addition of transport system; 5) co-option of the duplicated genes into C4 pathway and adaptive changes of C4 enzymes. Based on our current understanding on C4 evolution, several strategies for engineering C4 rice have been proposed to increase both photosynthetic efficiency and yield significantly in order to avoid international food crisis in the future, especially in the developing countries. Here we summarize the latest progresses on the studies of C4 evolution and discuss the strategies to introduce two-celled C4 pathway into rice.

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LEAF ANATOMY CHARACTERIZATION OF FOUR Apochloa SPECIES: A C3 GENUS RELATED TO EVOLUTION OF C4 PATHWAY IN GRASSES

Acta Biológica Colombiana ◽

10.15446/abc.v26n1.83228 ◽

2020 ◽

Vol 26 (1) ◽

pp. 12-18

Author(s):

Ane Marcela das Chagas Mendonça ◽

Pedro Lage Viana ◽

João Paulo Rodrigues Alves Delfino Barbosa

Keyword(s):

Leaf Anatomy ◽

C4 Photosynthesis ◽

Water Status ◽

Bundle Sheath ◽

C3 Plants ◽

Plant Water ◽

Kranz Anatomy ◽

C4 Pathway ◽

Photosynthesis Pathway

Leaf anatomy characteristics provide important evidences about the transition between C3 and C4 pathways. The C4 photosynthesis pathway allowed to reduce the C3 photorespiratory rate, concentrating CO2 around the Rubisco site and using structures and machinery already presented in C3 plants. In monocots, it is observed a high number of C4 lineages, most of them phylogenetically related to C3 groups. The genus Apochloa (C3), subtribe Arthropogoninae, is related to two C4 genera Coleataenia and Cyphonanthus. The aim of this study was to evaluate four Apochloa species in order to establish anatomical characteristics related to the evolution of C4 pathway in this group. By means of transverse sections fully expanded leaves of A. euprepes, A. lorea, A. molinioides, and A. poliophylla were collected and the characteristics of the mesophyll (M) and bundle sheath (BS) cells were determined. These species showed a rustic Kranz anatomy with enlarged and radial arranged BS cells, which have few organelles organized in a centrifugal position. Although the modifications of BS cells are probably related to the maintenance of plant water status, we also discuss the evolution for the establishment of C4 photosynthesis in the related C4 genera.

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Modelling metabolic evolution on phenotypic fitness landscapes: a case study on C4 photosynthesis

Biochemical Society Transactions ◽

10.1042/bst20150148 ◽

2015 ◽

Vol 43 (6) ◽

pp. 1172-1176 ◽

Cited By ~ 4

Author(s):

David Heckmann

Keyword(s):

Structural Changes ◽

Crop Yields ◽

C4 Photosynthesis ◽

Fitness Landscape ◽

Fitness Landscapes ◽

C3 Plants ◽

Metabolic Systems ◽

C4 Pathway ◽

Evolutionary Trajectories ◽

Phenotypic Fitness

How did the complex metabolic systems we observe today evolve through adaptive evolution? The fitness landscape is the theoretical framework to answer this question. Since experimental data on natural fitness landscapes is scarce, computational models are a valuable tool to predict landscape topologies and evolutionary trajectories. Careful assumptions about the genetic and phenotypic features of the system under study can simplify the design of such models significantly. The analysis of C4 photosynthesis evolution provides an example for accurate predictions based on the phenotypic fitness landscape of a complex metabolic trait. The C4 pathway evolved multiple times from the ancestral C3 pathway and models predict a smooth ‘Mount Fuji’ landscape accordingly. The modelled phenotypic landscape implies evolutionary trajectories that agree with data on modern intermediate species, indicating that evolution can be predicted based on the phenotypic fitness landscape. Future directions will have to include structural changes of metabolic fitness landscape structure with changing environments. This will not only answer important evolutionary questions about reversibility of metabolic traits, but also suggest strategies to increase crop yields by engineering the C4 pathway into C3 plants.

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C4 rice: a challenge for plant phenomics

Functional Plant Biology ◽

10.1071/fp09185 ◽

2009 ◽

Vol 36 (11) ◽

pp. 845 ◽

Cited By ~ 85

Author(s):

Robert T. Furbank ◽

Susanne von Caemmerer ◽

John Sheehy ◽

Gerry Edwards

Keyword(s):

C4 Photosynthesis ◽

Oryza Sativa L ◽

Yield Potential ◽

C3 Plants ◽

Or Efficiency ◽

C4 Pathway ◽

Large Populations ◽

Plant Phenomics ◽

Research Consortium ◽

Sorghum Bicolor L

There is now strong evidence that yield potential in rice (Oryza sativa L.) is becoming limited by ‘source’ capacity, i.e. photosynthetic capacity or efficiency, and hence the ability to fill the large number of grain ‘sinks’ produced in modern varieties. One solution to this problem is to introduce a more efficient, higher capacity photosynthetic mechanism to rice, the C4 pathway. A major challenge is identifying and engineering the genes necessary to install C4 photosynthesis in rice. Recently, an international research consortium was established to achieve this aim. Central to the aims of this project is phenotyping large populations of rice and sorghum (Sorghum bicolor L.) mutants for ‘C4-ness’ to identify C3 plants that have acquired C4 characteristics or revertant C4 plants that have lost them. This paper describes a variety of plant phenomics approaches to identify these plants and the genes responsible, based on our detailed physiological knowledge of C4 photosynthesis. Strategies to asses the physiological effects of the installation of components of the C4 pathway in rice are also presented.

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Are crassulacean acid metabolism and C4 photosynthesis incompatible?

Functional Plant Biology ◽

10.1071/pp01217 ◽

2002 ◽

Vol 29 (6) ◽

pp. 775 ◽

Cited By ~ 40

Author(s):

Rowan F. Sage

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

C4 Photosynthesis ◽

Bundle Sheath ◽

C4 Plants ◽

Cam Plants ◽

Bundle Sheath Cells ◽

C4 Pathway ◽

Cam Species ◽

Cam Photosynthesis

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. Despite sharing a similar metabolism, crassulacean acid metabolism (CAM) and C4 photosynthesis are not known to occur in identical species, with the exception of Portulaca spp. In Portulaca, C4 and weak CAM photosynthesis occur in distinct regions of the leaf, rather than in the same cells. This is in marked contrast to the situation in most CAM species where C3 and CAM photosynthesis are active in the same cell over the course of a day and growing season. The lack of CAM and C4 photosynthesis in identical cells of a plant indicates these photosynthetic pathways are incompatible. Incompatibilities between CAM and C4 photosynthesis could have a number of biochemical, anatomical and evolutionary explanations. Biochemical incompatibilities could result from the requirement for spatial separation of C3 and C4 phases in C4 plants versus temporal separation in CAM plants. In C4 plants, regulatory systems coordinate mesophyll and bundle sheath metabolism, with light intensity being the major environmental signal. In CAM plants, a circadian oscillator coordinates day and night phases of CAM. The requirement for rapid intercellular transport in C4 plants may be incompatible with the intracellular transport and storage needs of CAM. For example, the large vacuole required for malate storage in CAM could impede metabolite diffusion between mesophyll and bundle sheath cells in C4 plants. Anatomical barriers could also exist because both CAM and the C4 pathway require distinct leaf anatomies for efficient function. Efficient function of the C4 pathway generally requires an outer layer of cells specialized for phosphoenolpyruvate (PEP) carboxylation and regeneration and an inner layer for CO2 accumulation and refixation, while CAM species require enlarged vacuoles and tight cell packing. In evolutionary terms, barriers preventing CAM and C4 photosynthesis in the same species may be the initial steps in the respective evolutionary pathways from C3 ancestors. The first steps in C4 photosynthesis are related to scavenging photorespiratory CO2 via localization of glycine decarboxylase in the bundle sheath cells. The initial steps in CAM evolution are associated with the scavenging of respiratory CO2 at night by PEP carboxylation. In each, simplified versions of the specialized anatomy may need to be present for the evolutionary sequence to begin. For C4 evolution, enhanced bundle sheath size may be required in C3 ancestors; for CAM evolution, succulence may be required. Thus, before CAM or C4 photosynthesis began to evolve, the outcome of the evolutionary experiment may have been predetermined.

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Physiological, anatomical and biochemical characterisation of photosynthetic types in genus Cleome (Cleomaceae)

Functional Plant Biology ◽

10.1071/fp06287 ◽

2007 ◽

Vol 34 (4) ◽

pp. 247 ◽

Cited By ~ 41

Author(s):

Elena V. Voznesenskaya ◽

Nuria K. Koteyeva ◽

Simon D. X. Chuong ◽

Alexandra N. Ivanova ◽

João Barroca ◽

...

Keyword(s):

Leaf Anatomy ◽

C4 Photosynthesis ◽

C3 Plants ◽

Intermediate Species ◽

Δ13c Values ◽

C4 Species ◽

Cleome Gynandra ◽

The Family ◽

C3 Species ◽

C4 Pathway

C4 photosynthesis has evolved many times in 18 different families of land plants with great variation in leaf anatomy, ranging from various forms of Kranz anatomy to C4 photosynthesis occurring within a single type of photosynthetic cell. There has been little research on photosynthetic typing in the family Cleomaceae, in which only one C4 species has been identified, Cleome gynandra L. There is recent interest in selecting and developing a C4 species from the family Cleomaceae as a model C4 system, since it is the most closely related to Arabidopsis, a C3 model system (Brown et al. 2005). From screening more than 230 samples of Cleomaceae species, based on a measure of the carbon isotope composition (δ13C) in leaves, we have identified two additional C4 species, C. angustifolia Forssk. (Africa) and C. oxalidea F.Muell. (Australia). Several other species have δ13C values around –17‰ to –19‰, suggesting they are C4-like or intermediate species. Eight species of Cleome were selected for physiological, anatomical and biochemical analyses. These included C. gynandra, a NAD–malic enzyme (NAD–ME) type C4 species, C. paradoxa R.Br., a C3–C4 intermediate species, and 6 others which were characterised as C3 species. Cleome gynandra has C4 features based on low CO2 compensation point (Γ), C4 type δ13C values, Kranz-type leaf anatomy and bundle sheath (BS) ultrastructure, presence of C4 pathway enzymes, and selective immunolocalisation of Rubisco and phosphoenolpyruvate carboxylase. Cleome paradoxa was identified as a C3–C4 intermediate based on its intermediate Γ (27.5 μmol mol–1), ultrastructural features and selective localisation of glycine decarboxylase of the photorespiratory pathway in mitochondria of BS cells. The other six species are C3 plants based on Γ, δ13C values, non-Kranz leaf anatomy, and levels of C4 pathway enzymes (very low or absent) typical of C3 plants. The results indicate that this is an interesting family for studying the genetic basis for C4 photosynthesis and its evolution from C3 species.

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A synthetic C4 shuttle via the β-hydroxyaspartate cycle in C3 plants

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2022307118 ◽

2021 ◽

Vol 118 (21) ◽

pp. e2022307118

Author(s):

Marc-Sven Roell ◽

Lennart Schada von Borzykowski ◽

Philipp Westhoff ◽

Anastasija Plett ◽

Nicole Paczia ◽

...

Keyword(s):

C4 Photosynthesis ◽

Metabolic Process ◽

Growth And Yield ◽

C3 Plants ◽

Full Potential ◽

Bisphosphate Carboxylase ◽

Carbon And Nitrogen ◽

Energy Conserving ◽

Nitrogen Conservation ◽

Carbon Concentrating Mechanisms

Plants depend on the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) for CO2 fixation. However, especially in C3 plants, photosynthetic yield is reduced by formation of 2-phosphoglycolate, a toxic oxygenation product of Rubisco, which needs to be recycled in a high-flux–demanding metabolic process called photorespiration. Canonical photorespiration dissipates energy and causes carbon and nitrogen losses. Reducing photorespiration through carbon-concentrating mechanisms, such as C4 photosynthesis, or bypassing photorespiration through metabolic engineering is expected to improve plant growth and yield. The β-hydroxyaspartate cycle (BHAC) is a recently described microbial pathway that converts glyoxylate, a metabolite of plant photorespiration, into oxaloacetate in a highly efficient carbon-, nitrogen-, and energy-conserving manner. Here, we engineered a functional BHAC in plant peroxisomes to create a photorespiratory bypass that is independent of 3-phosphoglycerate regeneration or decarboxylation of photorespiratory precursors. While efficient oxaloacetate conversion in Arabidopsis thaliana still masks the full potential of the BHAC, nitrogen conservation and accumulation of signature C4 metabolites demonstrate the proof of principle, opening the door to engineering a photorespiration-dependent synthetic carbon–concentrating mechanism in C3 plants.

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