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Cereal Domestication and Evolution of Branching: Evidence for Soft Selection in the Tb1 Orthologue of Pearl Millet (Pennisetum glaucum [L.] R. Br.) Marie-Stanislas Remigereau 1,2¤a , Ghayas Lakis 1 , Samah Rekima 1 , Magalie Leveugle 1 , Michae ¨ l C. Fontaine 1 , Thierry Langin 2¤b , Aboubakry Sarr 1,3 , Thierry Robert 1,3 * 1 Laboratoire Ecologie, Syste ´ matique et Evolution, Universite ´ Paris-Sud XI, Orsay, France, 2 Institut de Biotechnologie des Plantes, Universite ´ Paris-Sud XI, Orsay, France, 3 Universite ´ Pierre et Marie Curie, Paris, France Abstract Background: During the Neolithic revolution, early farmers altered plant development to domest icate crops. Similar traits were often selected independently in different wild species; yet the genetic basis of this parallel phenotypic evolution remains elusive. Plant architecture ranks among these target traits composing the domestication syndrome. We focused on the reduction of branching which occurred in several cereals, an adaptation known to rely on the major gene Teosinte- branched1 (Tb1) in maize. We investigate the role of the Tb1 orthologue (Pgtb1) in the domestication of pearl millet (Pennisetum glaucum), an African outcrossing cereal. Methodology/P rincipal Findings: Gene cloning , expression profiling, QTL mappi ng and molecu lar evolution analysis were combined in a comparative approach between pearl millet and maize. Our results in pearl millet support a role for PgTb1 in domestication despite important differences in the genetic basis of branching adaptation in that species compared to maize (e.g. weaker effects of PgTb1). Genetic maps suggest this pattern to be consistent in other cereals with reduced branching (e.g. sorghum, foxtail millet). Moreover, although the adaptive sites underlying domestication were not formerly identified, signatu res of select ion pointed to putati ve regulatory regions upstream of both Tb1 orthologues in maize and pearl millet. However, the signature of human selection in the pearl millet Tb1 is much weaker in pearl millet than in maize. Conclusions/Significance: Our results suggest that some level of parallel evolution involved at least regions directly upstream of Tb1 for the domestication of pearl millet and maize. This was unanticipated given the multigenic basis of domestication traits and the divergence of wild progenitor species for over 30 million years prior to human selection. We also hypothesized that regular introgression of domestic pearl millet phenotypes by genes from the wild gene pool could explain why the selective sweep in pearl millet is softer than in maize. Citation: Remigereau M-S, Lakis G, Rekima S, Leveugle M, Fontaine MC, et al. (2011) Cereal Domestication and Evolution of Branching: Evidence for Soft Selection in the Tb1 Orthologue of Pearl Millet (Pennisetum glaucum [L.] R. Br.). PLoS ONE 6(7): e22404. doi:10.1371/journal.pone.0022404 Editor: Pa ¨ r K. Ingvarsson, University of Umea ˚, Sweden Received April 12, 2011; Accepted June 21, 2011; Published July 22, 2011 Copyright: 2011 Remigereau et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was funded by the ANR (Agence Nationale pour la Recherche Scientifique) Biodiversity program (ANR-06-BDIV-003-01) - project Transbiodiv, and by the Centre National de la Recherche Scientifique (CNRS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] ¤a Current address: Molecular and Computational Biology, University of Southern California, Los Angeles, California, United States of America ¤b Current address: Ge ´ ne ´ tique, Diversite ´ et Ecophysiologie des Ce ´ re ´ ales, Institut National de la Recherche Agronomique, Clermont-Ferrand, France Introduction Plant dome sti cati on prov ide s many exa mpl es of repeated phenotypic evolution [1,2] and a powerful system to explore its geneti c bas is [3,4]. Cereals in part icular sha re many common adapt at ions to cul ti vation which defi ne the domes ti cat ion syndrome [1,2]. They were domesticated from different wild grass species in distinct domestication centers 10,000 to 4,000 years ago [5]. Human selection focused on the seed and shaped the generally sma ll- siz ed, nat ura lly dis per sed and coa ted wil d see d int o the typ ical cereal grai n, large, naked, devoi d of dormancy and dispersal ability [5,6]. In maize, sorghum and millets (cereals of the Panicoideae subfamily), the characteristic bushy architecture of wil d progenitor spe cie s was als o alt ere d and bran ch number strongl y reduce d [7]. In maize in partic ular, vegetati ve branchi ng was almost comple tel y supp res sed (Fi gur e 1A) . The genetic dissection of these developmental adaptations in crosses between domesticated crops and their respective wild relatives has revealed that, despite the multig enic inheritan ce of domest icati on traits , some of the underlying quantitative trait loci (termed domestication QTL) coincide at conserved syntenic locations in the different cereal genomes. This has prompted the hypothesis that man could have unconscious ly and independen tly selected the same reper- toire of genes for the domestication of multiple species. This would constitute a large scale process of parallel genetic evolution [1], whereby repeat ed phenoty pi c evol uti on pro ceeded by the PLoS ONE | www.plosone.org 1 July 2011 | Volume 6 | Issue 7 | e22404

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