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The taxonomic distribution of C₄ photosynthesis in Amaranthaceae sensu stricto¹

Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2 Canada; Section of Evolution and Ecology, University of California, Davis, California 95616 USA; Nees-Institute for Biodiversity of Plants, Universität Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany

ABSTRACT

C₄ photosynthesis evolved multiple times in the Amaranthaceae s.s., but the C₄ evolutionary lineages are unclear because the photosynthetic pathway is unknown for most species of the family. To clarify the distribution of C₄ photosynthesis in the Amaranthaceae, we determined carbon isotope ratios of 607 species and mapped these onto a phylogeny determined from matK/trnK sequences. Approximately 28% of the Amaranthaceae species use the C₄ pathway. C₄ species occur in 10 genera—Aerva, Amaranthus, Blutaparon, Alternanthera, Froelichia, Lithophila, Guilleminea, Gomphrena, Gossypianthus, and Tidestromia. Aerva, Alternanthera, and Gomphrena contain both C₃ and C₄ species. In Aerva, 25% of the sampled species are C₄. In Alternanthera, 19.5% are C₄, while 89% of the Gomphrena species are C₄. Integration of isotope and matK/trnK data indicated C₄ photosynthesis evolved five times in the Amaranthaceae, specifically in Aerva, Alternanthera, Amaranthus, Tidestromia, and a lineage containing Froelichia, Blutaparon, Guilleminea, Gomphrena pro parte, and Lithophila. Aerva and Gomphrena are both polyphyletic with C₃ and C₄ species belonging to distinct clades. Alternanthera appears to be monophyletic with C₄ photosynthesis originating in a terminal sublineage of procumbent herbs. Alpine C₄ species were also identified in Alternanthera, Amaranthus, and Gomphrena, including one species (Gomphrena meyeniana) from 4600 m a.s.l.

Key Words: alpine • Alternanthera • Amaranthaceae • C₄ photosynthesis • Gomphrena

Received for publication January 19, 2007. Accepted for publication October 9, 2007.

FOOTNOTES

¹ The authors thank M. Nee and N. Tarnowsky of the New York Botanical Garden, J. Solomon of the Missouri Botanical Garden, S. Atkins and K. Vollesen of Kew Gardens, and E. Wood of the Arnold Arboretum and Grey Herbarium for assisting in the access to herbarium materials. S. Clemants of the Brooklyn Botanical Garden kindly provided pre-published species lists of many Amaranthaceae genera. M. Frohlich of the British Museum of Natural History provided specimens from the British Museum Herbarium. L. Craven of the Australian National Herbarium and D. Kubien of the University of New Brunswick provided specimens of Australian Gomphrena. The authors are grateful to K. Müller (Bonn) for providing an unpublished trnK/matK sequence for Amaranthus praetermissus, and to G. Kadereit (Mainz) and K. Wilhelm (Oldenburg) for valuable comments on an earlier version of the manuscript. Funding was provided by grants BO 1815/1–1 and 1–3 and a Heisenberg fellowship from the Deutsche Forschungsgemeinschaft (DFG) to T.B. and grant OGP-0154273 from the Natural Science and Engineering Council of Canada to R.F.S.

² Author for correspondence (e-mail: R.sage{at}utoronto.ca )

⁶ Current address: Plant Biodiversity and Evolution Group and Botanical Garden, Carl von Ossietzky Universität Oldenburg, 26111 Oldenburg, Germany

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