Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution1, 2, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines3. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes4, 5. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.
At a glance
Gene Expression Omnibus
- Linkage mapping of domestication loci in a large maize-teosinte backcross resource. Genetics 177, 1915–1928 (2007). , , &
- The effects of artificial selection of the maize genome. Science 308, 1310–1314 (2005). et al.
- Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. published online, doi:10.1038/ng.2313 (3 June 2012). et al.
- The evolution of apical dominance in maize. Nature 386, 485–488 (1997). , &
- The origin of the naked grains of maize. Nature 436, 714–719 (2005). et al.
- Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proc. Natl. Acad. Sci. USA 106, 5019–5024 (2009). , , , &
- A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl. Acad. Sci. USA 99, 6080–6084 (2002). et al.
- Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc. Natl. Acad. Sci. USA 108, 1088–1092 (2011). et al.
- Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3, 1745–1756 (2007). et al.
- Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053–1059 (2010). et al.
- Teosinte: The Closest Relative of Maize (The Bussey Institute of Harvard University, Cambridge, Massachusetts, 1967).
- Population differentiation as a test for selective sweeps. Genome Res. 20, 393–402 (2010). , &
- Megabase-scale inversion polymorphism in the wild ancestor of maize. Genetics published online, doi:10.1534/genetics.112.138578 (27 April 2012). et al.
- Archaeological data reveal slow rates of evolution during plant domestication. Evolution 65, 171–183 (2011). &
- Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173, 975–983 (2006). et al.
- Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc. Natl. Acad. Sci. USA 101, 9885–9890 (2004). , , &
- Maize adaptation to temperate climate: relationship between population structure and polymorphism in the Dwarf8 gene. Genetics 172, 2449–2463 (2006). et al.
- Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet. 7, e1002383 (2011). et al.
- The genetic architecture of maize flowering time. Science 325, 714–718 (2009). et al.
- An approach to the genetics of nitrogen use efficiency in maize. J. Exp. Bot. 55, 295–306 (2004). &
- Control of phyllotaxy in maize by the abphyl1 gene. Development 126, 315–323 (1999). &
- Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14, 1253–1263 (2002). et al.
- Green revolution: a mutant gibberellin-synthesis gene in rice—new insight into the rice variant that helped to avert famine over thirty years ago. Nature 416, 701–702 (2002). et al.
- Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J. 43, 413–424 (2005). et al.
- SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18, 665–675 (2006).
- Genome-wide atlas of transcription during maize development. Plant J. 66, 553–563 (2011). et al.
- Patterns of selection and tissue-specific expression among maize domestication and crop improvement loci. Plant Physiol. 144, 1642–1653 (2007). , , , &
- Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol. 8, 33 (2008). et al.
- Teosinte and the origin of maize. J. Hered. 30, 245–247 (1939).
- OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ. 32, 1412–1427 (2009). et al.
- A novel class of gibberellin 2–oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20, 2603–2618 (2008). et al.
- The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112–1115 (2009). et al.
- Genetic properties of the maize nested association mapping population. Science 325, 737–740 (2009). et al.
- Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic loci shaped primarily by retrotransposons. PLoS Genet. 5, e1000743 (2009). et al.
- libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19, 2325–2327 (2003).
- The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009). et al.
- A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9, 138–151 (1992). , &
- Two-locus sampling distributions and their application. Genetics 159, 1805–1817 (2001).
- Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. 20, 1689–1699 (2010). et al.
- Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264 (2003). et al.
- Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 5, e1000734 (2010). et al.
- MaizeGDB, the community database for maize genetics and genomics. Nucleic Acids Res. 32, D393–D397 (2004). , , , &
- Bootstrap Methods and Their Application (Cambridge University Press, New York, 1997). &