Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

Kapralov, Maxim V.; Smith, J. Andrew C.; Filatov, Dmitry A.

doi:10.1371/journal.pone.0052974

Cited by 54 publications

(75 citation statements)

References 63 publications

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“…With the exceptions of residues 469 and 477, these residues have been reported previously in other groups of plants, implying a relatively limited number of residues responsible for the Rubisco fine-tuning (Kapralov and Filatov, 2007;Christin et al, 2008;Iida et al, 2009;Kapralov et al, 2011Kapralov et al, , 2012Galmés et al, 2014aGalmés et al, , 2014c. However, despite widespread parallel evolution of amino acid replacements in the Rubisco sequence, solutions found in particular groups of plants may be quite different.…”

Section: The Analysis Of Positive Selection In Branches Leading To Spmentioning

confidence: 71%

Rubisco Catalytic Properties and Temperature Response in Crops

2016

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ORCID IDs: 0000-0003-3272-3054 (C.H.-C.); 0000-0001-7966-0295 (M.V.K.); 0000-0002-7299-9349 (J.G.).Rubisco catalytic traits and their thermal dependence are two major factors limiting the CO 2 assimilation potential of plants. In this study, we present the profile of Rubisco kinetics for 20 crop species at three different temperatures. The results largely confirmed the existence of significant variation in the Rubisco kinetics among species. Although some of the species tended to present Rubisco with higher thermal sensitivity (e.g. Oryza sativa) than others (e.g. Lactuca sativa), interspecific differences depended on the kinetic parameter. Comparing the temperature response of the different kinetic parameters, the Rubisco K m for CO 2 presented higher energy of activation than the maximum carboxylation rate and the CO 2 compensation point in the absence of mitochondrial respiration. The analysis of the Rubisco large subunit sequence revealed the existence of some sites under adaptive evolution in branches with specific kinetic traits. Because Rubisco kinetics and their temperature dependency were species specific, they largely affected the assimilation potential of Rubisco from the different crops, especially under those conditions (i.e. low CO 2 availability at the site of carboxylation and high temperature) inducing Rubisco-limited photosynthesis. As an example, at 25°C, Rubisco from Hordeum vulgare and Glycine max presented, respectively, the highest and lowest potential for CO 2 assimilation at both high and low chloroplastic CO 2 concentrations. In our opinion, this information is relevant to improve photosynthesis models and should be considered in future attempts to design more efficient Rubiscos.

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Section: The Analysis Of Positive Selection In Branches Leading To Spmentioning

confidence: 71%

Rubisco Catalytic Properties and Temperature Response in Crops

2016

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“…The software MODELTEST 3.7 (Posada and Crandall, 1998;Posada and Buckley, 2004) was used to check for the best model before running the phylogenetic analyses using maximum-likelihood inference conducted with RAxML version 7.2.6 (Stamatakis, 2006). Rubisco amino acid residues under positive selection associated with particular kinetic traits were identified using codon-based substitution models in comparative analysis of protein-coding DNA sequences within the phylogenetic framework using branch-site tests of positive selection along prespecified foreground branches in the PAML v.4.7 package (Yang, 2007) as described (Kapralov et al, , 2012Galmés et al, 2014b). Branches leading to species with high or low K c air , k cat c , K o , k cat o , and S C/O at 25°C were marked as foreground branches.…”

Section: Rubisco L-subunit Sites Under Positive Selectionmentioning

confidence: 99%

Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency

et al. 2016

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The threat to global food security of stagnating yields and population growth makes increasing crop productivity a critical goal over the coming decades. One key target for improving crop productivity and yields is increasing the efficiency of photosynthesis. Central to photosynthesis is Rubisco, which is a critical but often rate-limiting component. Here, we present full Rubisco catalytic properties measured at three temperatures for 75 plants species representing both crops and undomesticated plants from diverse climates. Some newly characterized Rubiscos were naturally "better" compared to crop enzymes and have the potential to improve crop photosynthetic efficiency. The temperature response of the various catalytic parameters was largely consistent across the diverse range of species, though absolute values showed significant variation in Rubisco catalysis, even between closely related species. An analysis of residue differences among the species characterized identified a number of candidate amino acid substitutions that will aid in advancing engineering of improved Rubisco in crop systems. This study provides new insights on the range of Rubisco catalysis and temperature response present in nature, and provides new information to include in models from leaf to canopy and ecosystem scale.

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“…To circumvent the difficulty in assaying Rubisco kinetic parameters, an alternative approach has been to analyze variation in DNA and amino acid sequences. Kapralov et al (2012) applied a phylogenetic analysis of Rubisco DNA sequence to identify which amino acids were selected during the evolution of C 4 photosynthesis in Amaranthaceae. Since this type of analysis relies on knowing that there are kinetic differences, it cannot be used to inform one of the properties of novel changes.…”

Section: Rubisco Kinetic Parametersmentioning

confidence: 99%

Improving Photosynthesis

2013

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Photosynthesis is the basis of plant growth, and improving photosynthesis can contribute toward greater food security in the coming decades as world population increases. Multiple targets have been identified that could be manipulated to increase crop photosynthesis. The most important target is Rubisco because it catalyses both carboxylation and oxygenation reactions and the majority of responses of photosynthesis to light, CO 2 , and temperature are reflected in its kinetic properties. Oxygenase activity can be reduced either by concentrating CO 2 around Rubisco or by modifying the kinetic properties of Rubisco. The C 4 photosynthetic pathway is a CO 2 -concentrating mechanism that generally enables C 4 plants to achieve greater efficiency in their use of light, nitrogen, and water than C 3 plants. To capitalize on these advantages, attempts have been made to engineer the C 4 pathway into C 3 rice (Oryza sativa). A simpler approach is to transfer bicarbonate transporters from cyanobacteria into chloroplasts and prevent CO 2 leakage. Recent technological breakthroughs now allow higher plant Rubisco to be engineered and assembled successfully in planta. Novel amino acid sequences can be introduced that have been impossible to reach via normal evolution, potentially enlarging the range of kinetic properties and breaking free from the constraints associated with covariation that have been observed between certain kinetic parameters. Capturing the promise of improved photosynthesis in greater yield potential will require continued efforts to improve carbon allocation within the plant as well as to maintain grain quality and resistance to disease and lodging.

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Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

Cited by 54 publications

References 63 publications

Rubisco Catalytic Properties and Temperature Response in Crops

Rubisco Catalytic Properties and Temperature Response in Crops

Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency

Improving Photosynthesis

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