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J Exp Bot. 2014 Jul;65(13):3609-21. doi: 10.1093/jxb/eru087. Epub 2014 Mar 17.

Shared origins of a key enzyme during the evolution of C4 and CAM metabolism.

Author information

1
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman St., Providence, RI 02912, USA p.christin@sheffield.ac.uk.
2
Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman St., Providence, RI 02912, USA Departamento de Botánica, Facultad de Ciencias Biológicas and Museo de Historia Natural - UNMSM, Av. Arenales 1256, Lima 11, Peru.
3
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK.
4
Institute of Plant Biochemistry, Heinrich-Heine University, 40225 Duesseldorf, Germany.
5
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada.
6
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK.
7
Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK.
8
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada Department of Medicine, University of Alberta, Edmonton, Alberta T6G 2E1, Canada BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen 518083, China.
9
Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman St., Providence, RI 02912, USA.

Abstract

CAM and C4 photosynthesis are two key plant adaptations that have evolved independently multiple times, and are especially prevalent in particular groups of plants, including the Caryophyllales. We investigate the origin of photosynthetic PEPC, a key enzyme of both the CAM and C4 pathways. We combine phylogenetic analyses of genes encoding PEPC with analyses of RNA sequence data of Portulaca, the only plants known to perform both CAM and C4 photosynthesis. Three distinct gene lineages encoding PEPC exist in eudicots (namely ppc-1E1, ppc-1E2 and ppc-2), one of which (ppc-1E1) was recurrently recruited for use in both CAM and C4 photosynthesis within the Caryophyllales. This gene is present in multiple copies in the cacti and relatives, including Portulaca. The PEPC involved in the CAM and C4 cycles of Portulaca are encoded by closely related yet distinct genes. The CAM-specific gene is similar to genes from related CAM taxa, suggesting that CAM has evolved before C4 in these species. The similar origin of PEPC and other genes involved in the CAM and C4 cycles highlights the shared early steps of evolutionary trajectories towards CAM and C4, which probably diverged irreversibly only during the optimization of CAM and C4 phenotypes.

KEYWORDS:

C4 photosynthesis; CAM photosynthesis; co-option; evolution; phosphoenolpyruvate carboxylase (PEPC); phylogenetics.

PMID:
24638902
PMCID:
PMC4085957
DOI:
10.1093/jxb/eru087
[Indexed for MEDLINE]
Free PMC Article

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