DOI: 10.1126/science.1089056 , 1206 (2003) 302 Science et al. Viviane Jaenicke-Despr��s, Early Allelic Selection in Maize as Revealed by Ancient DNA This copy is for your personal, non-commercial use only. clicking here. colleagues, clients, or customers by , you can order high-quality copies for your If you wish to distribute this article to others here. following the guidelines can be obtained by Permission to republish or repurpose articles or portions of articles ): November 8, 2011 www.sciencemag.org (this infomation is current as of The following resources related to this article are available online at http://www.sciencemag.org/content/302/5648/1206.full.html version of this article at: including high-resolution figures, can be found in the online Updated information and services, http://www.sciencemag.org/content/suppl/2003/11/13/302.5648.1206.DC1.html can be found at: Supporting Online Material http://www.sciencemag.org/content/302/5648/1206.full.html#related found at: can be related to this article A list of selected additional articles on the Science Web sites 67 article(s) on the ISI Web of Science cited by This article has been http://www.sciencemag.org/content/302/5648/1206.full.html#related-urls 28 articles hosted by HighWire Press see: cited by This article has been http://www.sciencemag.org/cgi/collection/evolution Evolution subject collections: This article appears in the following registered trademark of AAAS. is a Science 2003 by the American Association for the Advancement of Science all rights reserved. The title Copyright American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075 online ISSN 1095-9203) is published weekly, except the last week in December, by the Science on November 8, 2011 www.sciencemag.org Downloaded from

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We have analyzed three genes involved in the control of plant architecture, storage protein synthesis, and starch production from archaeological maize samples from Mexico and the southwestern United States. The results reveal that the alleles typical of contemporary maize were present in Mexican maize by 4400 years ago. However, as recently as 2000 years ago, allelic selection at one of the genes may not yet have been complete. The wild grass, teosinte (Zea mays ssp. parvi- glumis), from which maize (Zea mays ssp. mays) was domesticated, is endemic to southern and western Mexico (1). The earliest undisputed ar- chaeological evidence of domesticated maize is 6250 years old (2). However, recent molecular data suggest that domestication could have be- gun as early as 9000 years ago and that the Balsas River Valley in southern Mexico is the likely geographical origin of domestication (3). The early history of character selection in maize is documented in the archaeological record by morphological features discernible in cobs. For example, an increase in the number of rows of kernels and a reduction in glume size have been noted in early maize cobs (4). By 5500 years ago, kernel size had also increased (5). However, nothing is currently known about when charac- ters not observable from the morphology of cobs, such as plant architecture and starch prop- erties, were selected by early farmers. Recently, a number of genetic loci as- sociated with phenotypic differences be- tween maize and teosinte have been iden- tified (6���9), and three genes involved in such differences have been cloned and rel- atively well characterized in function (7, 9, 10). In each of these genes, the allelic diversity in maize compared with teosinte has been shown to be reduced, presumably as a result of selection by early farmers. The first gene, teosinte branched 1 (tb1), carries a maize variant that represses the growth in axillary meristems, leading to the unbranched plant architecture typical of maize. It also contributes to the presence of female cobs on the primary branches in maize rather than male tassels as in teosinte (11, 12). The second gene encodes the pro- lamin box binding factor (pbf), which is involved in the control of expression of seed storage proteins in the kernel (13���15), whereas the third gene, sugary 1 (su1), encodes a starch debranching enzyme ex- pressed in kernels (16). Together with branching enzymes, this enzyme deter- mines the structure of amylopectin (16, 17 ). The chain length of amylopectin, as well as the ratio of amylose to amylopectin, is important for the gelatinization proper- ties of starch (9) and, thus, affects the textural properties of tortillas (18, 19). Because DNA in archaeological remains is generally degraded to small sizes (20), we identified fragments in each gene that are short enough to allow amplification from an- cient corn cobs yet distinguish between the spectrum of gene variants (alleles) found in present-day maize and teosinte (10). For tb1, the allelic variation in contemporary maize and teosinte is well described (10). This al- lowed us to choose a fragment of 56 base pairs (bp) for which maize carries a single allele, Tb1-M1 this allele has a frequency of 36% in teosinte, where a total of six addition- al alleles exist. In order to characterize the contemporary variation in pbf and su1, we sequenced a longer segment of each gene in 66 maize landraces from South, Middle, and North America as well as 23 teosinte parvi- glumis lines (10). The estimated number of alleles segregating in maize is reduced about threefold at pbf and su1 in comparison to teosinte (fig. S1, B and C). At pbf, we select- ed a 25-bp fragment in which the alleles Pbf-M1 and Pbf-M2 are carried in 97% and 3% of maize, whereas the same alleles are carried in 17% and 83% of teosinte, respec- tively (Fig. 1). At su1, we selected a 60-bp fragment in which two major alleles, Su1-M1 and Su1-M2, are carried in maize at a fre- quency of 30 and 62%, respectively, whereas they both are carried in teosinte at a frequen- cy of about 7% (Fig. 1 table S2) (10). We investigated five maize cobs from the Ocampo Caves in northeastern Mexico (Fig. 2) and six cobs from Tularosa Cave in the Mogollon highlands in New Mexico (10). 1Max Planck-Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany. 2United States Department of Agriculture/Agricultural Re- search Service and Department of Genetics, North Carolina State University, Raleigh, NC 27695, USA. 3Archaeobiology Program, Department of Anthropol- ogy, National Museum of Natural History, Smithso- nian Institution, Washington, DC 20560, USA. 4Henry Wellcome Ancient Biomolecules Centre, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK. 5Laboratory of Genetics, University of Wisconsin, Madison, WI 53706, USA. *To whom correspondence should be addressed. E- mail: paabo@eva.mpg.de R E P O R T S 14 NOVEMBER 2003 VOL 302 SCIENCE www.sciencemag.org 1206 on November 8, 2011 www.sciencemag.org Downloaded from