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The genetics of convergent evolution: insights from plant photosynthesis

Abstract

The tree of life is resplendent with examples of convergent evolution, whereby distinct species evolve the same trait independently. Many highly convergent adaptations are also complex, which makes their repeated emergence surprising. In plants, the evolutionary history of two carbon concentrating mechanisms (CCMs) — C4 and crassulacean acid metabolism (CAM) photosynthesis — presents such a paradox. Both of these modifications of ancestral C3 photosynthesis require the integration of multiple anatomical and biochemical components, yet together they have evolved more than one hundred times. The presence of CCM enzymes in all plants suggests that a rudimentary CCM might emerge via relatively few genetic changes in potentiated lineages. Here, we propose that many of the complexities often associated with C4 and CAM photosynthesis may have evolved during a post-emergence optimization phase. The ongoing development of new model clades for young, emerging CCMs is enabling the comparative studies needed to test these ideas.

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Acknowledgements

The authors thank members of the Edwards laboratory for their thoughtful discussions on this manuscript. K.H. is supported by a Donnelley Postdoctoral Fellowship through the Yale Institute of Biospheric Studies. Additional support came from US National Science Foundation awards DEB-1252901 and IOS-1754662 to E.J.E. P.-A.C. is supported by a Royal Society Research Fellowship (grant number URF120119).

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Nature Reviews Genetics thanks R. VanBuren and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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The authors contributed equally to all aspects of the article.

Correspondence to Karolina Heyduk.

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Glossary

Anaplerotic

Chemical reactions that provide intermediates to various metabolic pathways, including the tricarboxylic acid (TCA) cycle.

Carboxylation

The addition of a carboxyl group to a substrate, often via a carboxylase enzyme.

Co-option

The recruitment of a gene, enzyme or other trait for an alternative function.

Decarboxylated

Pertaining to a molecule from which a carboxyl group has been removed by a decarboxylase enzyme in a process that releases CO2.

Duons

Portions of the genome that both code for amino acids and provide motifs that can regulate gene expression.

Gene flow

Movement of genetic information between populations.

Genome-wide association studies

Analyses that correlate genetic markers from across the genome with a phenotype of interest in order to find loci underlying traits.

Lateral gene transfer

Movement of genes between individuals by mechanisms other than sexual reproduction.

Photorespiration

Fixation of oxygen by Rubisco, resulting in a loss of energy and a release of CO2 but no net gain in carbohydrates.

Transpiration

The passive movement of water via stomata from the leaf intercellular airspace to the atmosphere along the water concentration gradient.

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Further reading

Fig. 1: Biochemistry of C3 and CCM pathways.
Fig. 2: Evolutionary patterns of CCMs.
Fig. 3: Expression of PEPC in the leaves of C3 angiosperms belonging to CCM-evolving lineages.