Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Roell MS

PROVIDER: S-EPMC8166194 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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

Roell Marc-Sven MS Schada von Borzykowski Lennart L Westhoff Philipp P Plett Anastasija A Paczia Nicole N Claus Peter P Urte Schlueter S Erb Tobias J TJ Weber Andreas P M APM

Proceedings of the National Academy of Sciences of the United States of America 20210501 21

Plants depend on the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) for CO<sub>2</sub> 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 mechanism ...[more]

PMID: 34001608

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Project description:BackgroundThe C4 photosynthetic cycle supercharges photosynthesis by concentrating CO2 around ribulose-1,5-bisphosphate carboxylase and significantly reduces the oxygenation reaction. Therefore engineering C4 feature into C3 plants has been suggested as a feasible way to increase photosynthesis and yield of C3 plants, such as rice, wheat, and potato. To identify the possible transition from C3 to C4 plants, the systematic comparison of C3 and C4 metabolism is necessary.ResultsWe compared C3 and C4 metabolic networks using the improved constraint-based models for Arabidopsis and maize. By graph theory, we found the C3 network exhibit more dense topology structure than C4. The simulation of enzyme knockouts demonstrated that both C3 and C4 networks are very robust, especially when optimizing CO2 fixation. Moreover, C4 plant has better robustness no matter the objective function is biomass synthesis or CO2 fixation. In addition, all the essential reactions in C3 network are also essential for C4, while there are some other reactions specifically essential for C4, which validated that the basic metabolism of C4 plant is similar to C3, but C4 is more complex. We also identified more correlated reaction sets in C4, and demonstrated C4 plants have better modularity with complex mechanism coordinates the reactions and pathways than that of C3 plants. We also found the increase of both biomass production and CO2 fixation with light intensity and CO2 concentration in C4 is faster than that in C3, which reflected more efficient use of light and CO2 in C4 plant. Finally, we explored the contribution of different C4 subtypes to biomass production by setting specific constraints.ConclusionsAll results are consistent with the actual situation, which indicate that Flux Balance Analysis is a powerful method to study plant metabolism at systems level. We demonstrated that in contrast to C3, C4 plants have less dense topology, higher robustness, better modularity, and higher CO2 and radiation use efficiency. In addition, preliminary analysis indicated that the rate of CO2 fixation and biomass production in PCK subtype are superior to NADP-ME and NAD-ME subtypes under enough supply of water and nitrogen.

Project description:A wide range of C3 and C4 plant species could acclimatize and grow under the impact of salinity stress. Symbiotic relationship between plant roots and arbuscular mycorrhizal fungi (AMF) are widespread and are well known to ameliorate the influence of salinity stress on agro-ecosystem. In the present study, we sought to understand the phenomenon of variability on AMF symbiotic relationship on saline stress amelioration in C3 and C4 plants. Thus, the objective was to compare varied mycorrhizal symbiotic relationship between C3 and C4 plants in saline conditions. To accomplish the above mentioned objective, we conducted a random effects models meta-analysis across 60 published studies. An effect size was calculated as the difference in mycorrhizal responses between the AMF inoculated plants and its corresponding control under saline conditions. Responses were compared between (i) identity of AMF species and AMF inoculation, (ii) identity of host plants (C3 vs. C4) and plant functional groups, (iii) soil texture and level of salinity and (iv) experimental condition (greenhouse vs. field). Results indicate that both C3 and C4 plants under saline condition responded positively to AMF inoculation, thereby overcoming the predicted effects of symbiotic efficiency. Although C3 and C4 plants showed positive effects under low (EC < 4 ds/m) and high (>8 ds/m) saline conditions, C3 plants showed significant effects for mycorrhizal inoculation over C4 plants. Among the plant types, C4 annual and perennial plants, C4 herbs and C4 dicot had a significant effect over other counterparts. Between single and mixed AMF inoculants, single inoculants Rhizophagus irregularis had a positive effect on C3 plants whereas Funneliformis mosseae had a positive effect on C4 plants than other species. In all of the observed studies, mycorrhizal inoculation showed positive effects on shoot, root and total biomass, and in nitrogen, phosphorous and potassium (K) uptake. However, it showed negative effects in sodium (Na) uptake in both C3 and C4 plants. This influence, owing to mycorrhizal inoculation, was significantly higher in K uptake in C4 plants. For our analysis, we concluded that AMF-inoculated C4 plants showed more competitive K(+) ions uptake than C3 plants. Therefore, maintenance of high cytosolic K(+)/Na(+) ratio is a key feature of plant salt tolerance. Studies on the detailed mechanism for the selective transport of K in C3 and C4 mycorrhizal plants under salt stress is lacking, and this needs to be explored.

Project description:C4 photosynthesis is a carbon-concentrating mechanism that evolved independently more than 60 times in a wide range of angiosperm lineages. Among other alterations, the evolution of C4 from ancestral C3 photosynthesis requires changes in the expression of a vast number of genes. Differential gene expression analyses between closely related C3 and C4 species have significantly increased our understanding of C4 functioning and evolution. In Chenopodiaceae, a family that is rich in C4 origins and photosynthetic types, the anatomy, physiology and phylogeny of C4, C2, and C3 species of Salsoleae has been studied in great detail, which facilitated the choice of six samples of five representative species with different photosynthetic types for transcriptome comparisons. mRNA from assimilating organs of each species was sequenced in triplicates, and sequence reads were de novo assembled. These novel genetic resources were then analyzed to provide a better understanding of differential gene expression between C3, C2 and C4 species. All three analyzed C4 species belong to the NADP-ME type as most genes encoding core enzymes of this C4 cycle are highly expressed. The abundance of photorespiratory transcripts is decreased compared to the C3 and C2 species. Like in other C4 lineages of Caryophyllales, our results suggest that PEPC1 is the C4-specific isoform in Salsoleae. Two recently identified transporters from the PHT4 protein family may not only be related to the C4 syndrome, but also active in C2 photosynthesis in Salsoleae. In the two populations of the C2 species S. divaricata transcript abundance of several C4 genes are slightly increased, however, a C4 cycle is not detectable in the carbon isotope values. Most of the core enzymes of photorespiration are highly increased in the C2 species compared to both C3 and C4 species, confirming a successful establishment of the C2 photosynthetic pathway. Furthermore, a function of PEP-CK in C2 photosynthesis appears likely, since PEP-CK gene expression is not only increased in S. divaricata but also in C2 species of other groups.

Dataset Information

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

Publications

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

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