The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants

Niklaus, Michael; Kelly, Steven

doi:10.1093/jxb/ery416

Cited by 27 publications

(23 citation statements)

References 80 publications

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“…The CO 2 pump generated by the C 4 cycle of A. semialata is less efficient than that of other C 4 species (Niklaus and Kelly, 2019), as illustrated by the incomplete segregation of enzymes between different cell types (Ueno and Sentoku, 2006) and slightly elevated CO 2 compensation points lying at the upper limit of those observed in C 4 species (Lundgren et al , 2016). Therefore, A. semialata may be considered to exhibit an incipient C 4 cycle, which has not been optimized through protracted evolutionary periods, as suggested in the most recent models (Bräutigam and Gowik, 2016).…”

Section: Discussionmentioning

confidence: 99%

Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata

Dunning

Moreno-Villena

Lundgren

et al. 2019

Journal of Experimental Botany

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C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared with C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a single species, the grass Alloteropsis semialata, to detect changes in gene expression associated with different photosynthetic phenotypes. Phylogenetically informed comparative transcriptomics show that intermediates with a weak C4 cycle are separated from the C3 phenotype by increases in the expression of 58 genes (0.22% of genes expressed in the leaves), including those encoding just three core C4 enzymes: aspartate aminotransferase, phosphoenolpyruvate carboxykinase, and phosphoenolpyruvate carboxylase. The subsequent transition to full C4 physiology was accompanied by increases in another 15 genes (0.06%), including only the core C4 enzyme pyruvate orthophosphate dikinase. These changes probably created a rudimentary C4 physiology, and isolated populations subsequently improved this emerging C4 physiology, resulting in a patchwork of expression for some C4 accessory genes. Our work shows how C4 assembly in A. semialata happened in incremental steps, each requiring few alterations over the previous step. These create short bridges across adaptive landscapes that probably facilitated the recurrent origins of C4 photosynthesis through a gradual process of evolution.

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Section: Discussionmentioning

confidence: 99%

Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata

Dunning

Moreno-Villena

Lundgren

et al. 2019

Journal of Experimental Botany

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“…The C 4 photosynthetic mechanism is a classic example of convergent evolution, having evolved more than 60 times independently in various groups of flowering plants (Sage et al, 2011). As all known C 4 enzymes exist in C 3 plants, the evolution of C 4 photosynthesis involved the co-option of genes and proteins essential for the cycle followed by adaption of their expression levels and, at least in some cases, their kinetic properties (Blasing et al, 2002;Tausta et al, 2002;Ghannoum et al, 2005;Aubry et al, 2011;Christin et al, 2013;Heckmann et al, 2013;Kulahoglu et al, 2014;Huang et al, 2017;Moreno-Villena et al, 2018;Alvarez et al, 2019;Niklaus and Kelly, 2019). In particular, the transcript level, enzyme abundance and activity of PEPC are massively increased in all C 4 lineages screened so far (Engelmann et al, 2003;Marshall et al, 2007;Bräutigam et al, 2014;Christin et al, 2015;Moreno-Villena et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Kinetic Modifications of C4 PEPC Are Qualitatively Convergent, but Larger in Panicum Than in Flaveria

2020

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C 4 photosynthesis results from a set of anatomical features and biochemical components that act together to concentrate CO 2 within the leaf and boost productivity. This complex trait evolved independently many times, resulting in various realizations of the phenotype, but in all C 4 plants the primary fixation of atmospheric carbon is catalyzed by phosphoenolpyruvate carboxylase. Comparisons of C 4 and non-C 4 PEPC from a few closely related species suggested that the enzyme was modified to meet the demands of the C 4 cycle. However, very few C 4 groups have been investigated, hampering general conclusions. To test the hypothesis that distant C 4 lineages underwent convergent biochemical changes, we compare the kinetic variation between C 4 and non-C 4 PEPC from a previously assessed young lineage (Flaveria, Asteraceae) with those from an older lineage found within the distantly related grass family (Panicum). Despite the evolutionary distance, the kinetic changes between the non-C 4 and C 4 PEPC are qualitatively similar, with a decrease in sensitivity for inhibitors, an increased specificity (k cat /K m) for bicarbonate, and a decreased specificity (k cat /K m) for PEP. The differences are more pronounced in the older lineage Panicum, which might indicate that optimization of PEPC for the C 4 context increases with evolutionary time.

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“…In the C 3 photosynthesis, which is the most ancestral form, the enzyme ribulose bisphosphate carboxylaseoxygenase (RuBisCO) 5 , which is present in the chloroplast stroma of C 3 plants, combines the ribulose-1,5-bisphosphate (RuBP), a molecule containing five carbon atoms, with CO 2 to form two molecules of phosphoglycerate (PGA, a 3-carbon molecule) 6,7 . In the C 4 pathway, the CO 2 is converted into bicarbonate, which is subsequently reacted with phosphoenolpyruvic acid (PEP), a 3-carbon molecule, in the presence of phosphoenolpyruvate carboxylase (PEPC) 8 . The product of this reaction is a 4-carbon molecule, oxaloacetic acid (OAA), which is thereafter reduced to malate, another four-carbon acid 8 .…”

Section: Introductionmentioning

confidence: 99%

“…In the C 4 pathway, the CO 2 is converted into bicarbonate, which is subsequently reacted with phosphoenolpyruvic acid (PEP), a 3-carbon molecule, in the presence of phosphoenolpyruvate carboxylase (PEPC) 8 . The product of this reaction is a 4-carbon molecule, oxaloacetic acid (OAA), which is thereafter reduced to malate, another four-carbon acid 8 . The CAM pathway was documented for the first time in plant families that are adapted to very arid regions, such as many epiphytes and succulents 9 .…”

Section: Introductionmentioning

confidence: 99%

Use of an immobilised thermostable α-CA (SspCA) for enhancing the metabolic efficiency of the freshwater green microalga Chlorella sorokiniana

Salbitani

Prete

Bolinesi

et al. 2020

Journal of Enzyme Inhibition and Medicinal Chemistry

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The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants

Cited by 27 publications

References 80 publications

Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata

Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata

Kinetic Modifications of C4 PEPC Are Qualitatively Convergent, but Larger in Panicum Than in Flaveria

Use of an immobilised thermostable α-CA (SspCA) for enhancing the metabolic efficiency of the freshwater green microalga Chlorella sorokiniana

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