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. 2016 Dec 6;113(49):14151-14156.
doi: 10.1073/pnas.1609701113. Epub 2016 Nov 21.

The Earliest Maize From San Marcos Tehuacán Is a Partial Domesticate With Genomic Evidence of Inbreeding

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The Earliest Maize From San Marcos Tehuacán Is a Partial Domesticate With Genomic Evidence of Inbreeding

Miguel Vallebueno-Estrada et al. Proc Natl Acad Sci U S A. .
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Abstract

Pioneering archaeological expeditions lead by Richard MacNeish in the 1960s identified the valley of Tehuacán as an important center of early Mesoamerican agriculture, providing by far the widest collection of ancient crop remains, including maize. In 2012, a new exploration of San Marcos cave (Tehuacán, Mexico) yielded nonmanipulated maize specimens dating at a similar age of 5,300-4,970 calibrated y B.P. On the basis of shotgun sequencing and genomic comparisons to Balsas teosinte and modern maize, we show herein that the earliest maize from San Marcos cave was a partial domesticate diverging from the landraces and containing ancestral allelic variants that are absent from extant maize populations. Whereas some domestication loci, such as teosinte branched1 (tb1) and brittle endosperm2 (bt2), had already lost most of the nucleotide variability present in Balsas teosinte, others, such as teosinte glume architecture1 (tga1) and sugary1 (su1), conserved partial levels of nucleotide variability that are absent from extant maize. Genetic comparisons among three temporally convergent samples revealed that they were homozygous and identical by descent across their genome. Our results indicate that the earliest maize from San Marcos was already inbred, opening the possibility for Tehuacán maize cultivation evolving from reduced founder populations of isolated and perhaps self-pollinated individuals.

Keywords: Tehuacán; domestication; maize; paleogenomics; teosinte.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
New archeological excavations in San Marcos cave. (A) The caves of San Marcos (cave on the left) and Tecorral (cave on the right). (B) Archaeobotanical sampling in San Marcos cave conducted in February 2012. (C) Maize specimens SM3 dating 5,280–4,970 cal. y B.P. (Left) and SM5 dating 5,300–4,980 calibrated y B.P. (Right). (Scale bar, 1.5 cm.) (D) Maize specimens SM9 dating 5,280–4,970 cal. y B.P. (Left) and SM10 5,300–5,040 cal. y B.P. (Right). (Scale bar, 43 mm.)
Fig. 2.
Fig. 2.
Evolutionary relationships between ancient Tehuacán maize and its wild or cultivated relatives. ML tree from an alignment of 100,540 genome-wide SNPs covering nonrepetitive regions of the reference maize genome. SM3 and SM10 represent two maize samples dating 5,300–4,970 calibrated y B.P.; SNPs obtained from 77,960,582 mapped reads of the Palomero Toluqueño landrace (PT2233) were also included. The teosinte group is highlighted in green, the maize landrace group in red, and ancient maize samples from San Marcos in blue. The teosinte and landrace accessions follow previously reported nomenclatures (29); full details of bootstrap values are given in SI Appendix, Fig. S4.
Fig. 3.
Fig. 3.
Genomic evidence of partial domestication in ancient Tehuacán maize. Admixture diagrams comparing SM10 nonconsecutive nucleotide variants to the corresponding SNP frequencies reported in modern maize or Balsas teosinte accessions, over 20-kb intervals spanning a selected gene affected by domestication. Blue and yellow correspond to predominant nucleotide variants in extant maize (EM) and their match in SM10 ancient maize (AM) and Balsas teosinte (BT); additional variants in Balsas teosinte or SM10 are depicted in variable colors. Chromosomal locations are indicated adjacent to the locus acronym, in parenthesis; the horizontal scale shows the chromosomal coordinates following the B73 reference genome, and the location and transcriptional orientation of the corresponding gene (red arrow).

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