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First published online November 20, 2009; doi:10.3732/ajb.0900111 American Journal of Botany 96: 2234-2239 (2009) © 2009 Botanical Society of America, Inc.

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Two independent C₄ origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes¹

² Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland ³ Imperial College Silwood Park Campus, Buckhurst Road Ascot, Berkshire SL5 7PY, UK

ABSTRACT

Determining the number of evolutions of an adaptive novelty is primordial to understand its evolutionary significance. C₄ photosynthesis, an adaptation to low CO₂ atmospheric concentration and high temperature, evolved multiple times, but the number of convergent evolutions is still debated. In Poaceae phylogeny, numerous C₄ groups are separated by C₃ taxa, but whether these correspond to independent C₄ origins or a few C₄ evolutions followed by reversals is controversial. The Aristidoideae subfamily is formed by two C₄ genera, Aristida and Stipagrostis, separated by the C₃ genus Sartidia. In the current study, we investigated the evolutionary history of genes encoding phosphoenolpyruvate carboxylases (PEPC) to shed light on the photosynthetic transitions that occurred in Aristidoideae. We identified six distinct PEPC gene lineages that appeared through several rounds of gene duplications before or early during grass diversification. The gene lineage encoding the C₄ PEPC of Stipagrostis differs from those of the other C₄ grasses, including Aristida. These distinct origins of C₄ PEPC genes from these two Aristidoideae genera unequivocally indicate that they integrated the C₄ pathway independently. This highlights the importance of candidate-gene studies when inferring the evolutionary history of a character such as C₄ photosynthesis, one of the greatest evolutionary successes in plant history.

Key Words: Aristida • Aristidoideae • C₄ photosynthesis • character mapping • grasses • molecular evolution • multiple origins • phylogeny • Poaceae • Stipagrostis

Received for publication 20 April 2009. Accepted for publication 3 September 2009.

FOOTNOTES

¹ This work was funded by the Swiss NSF grant 3100AO-105886.G. B. was funded by the Intra-European fellowship PIEF-GA-2008-220813.The authors are especially grateful to Zuzana Khodlová and Emanuela Samaritani for their help in the laboratory and to Lucie Büchi for useful comments on an earlier version of this manuscript.

⁴ Author for correspondence (e-mail: Pascal-Antoine.Christin{at}unil.ch)

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