1 Kernel Evolution: from Teosinte to Maize

1 Kernel Evolution: From Teosinte to Maize Sherry A. Flint-Garcia* U.S. Department of Agriculture, Agricultural Research Service, Columbia, Missouri 1.1 Introduction 1.2 Domestication Maize is the most productive and highest Maize, like all the world’s major agricultural value commodity crop in the U.S. and crop plant and animal species, underwent around the world: over 1 billion tons were domestication from a wild relative. The produced each year in 2013 and 2014 (FAO, suite of phenotypic traits that were modified 2016). Together, maize, rice, and wheat during domestication is referred to as the comprise over 60% of the world’s caloric “domestication syndrome” (Hammer, 1984) intake (http://www.fao.org). The import- and usually includes traits related to prod- ance of maize in terms of production and uctivity (e.g. increased seed number and caloric intake is not a recent development. size), harvestability (e.g. non-shattering and In fact, Native Americans have relied on fewer seed-bearing structures), and con- maize and its ancestor for more than 9000 sumption (reduced toxicity and improved years. The “Columbian exchange” allowed palatability) among other species-specific maize to spread around the world, to adapt traits (Olsen and Wendel, 2013). Evolution to new environments and become a major of the seed was central to domestication, as crop that feeds large portions of the human were traits facilitating harvest. population. Maize, and the kernel in par- Genetic and archeological evidence ticular, has undergone dramatic changes suggest maize was domesticated from teo- over the past 9000 years. The biology of sinte (Zea mays ssp. parviglumis) approxi- maize seed size and its starch, protein, oil mately 9000 years ago in the Central Balsas content, and food characteristics, are de- River Valley in southwestern Mexico in the scribed in other chapters of this book. Here states of Guerrero and Michoacán (Matsuoka I review the evolution of maize from teosinte et al., 2002; Piperno et al., 2009). Zea mays (the wild ancestor) to landraces ( locally ssp. parviglumis (hereafter parviglumis) is adapted, open-pollinated farmer varieties) an annual diploid species endemic to south- to modern maize (inbreds and hybrids), and western Mexico (Doebley and Iltis, 1980). discuss changes in kernel composition and There are several other species of teosinte size during this process. with different ploidy levels, perenniality, *Corresponding author e-mail: [email protected] © CAB International 2017. 1 0003169069.INDD 1 7/21/2017 6:20:28 AM 2 S.A. Flint-Garcia and/or special regional adaptation to higher with a single stalk and short lateral branches elevations or lower latitudes (Fukunaga (ear shanks) ending in female inflorescences et al., 2005), but these will not be discussed (Fig. 1.1B). Teosinte plants are capable of in any detail. Hereafter, whenever teosinte is producing over 100 ear structures, each of mentioned, the reader may assume parviglu- which is comprised of 5 to 12 seeds stacked mis unless otherwise noted. and without a cob (Fig. 1.1C). Modern maize There are dramatic differences in plant, plants usually produce one or two ears with ear, and kernel morphology between maize cobs that bear several hundred kernels in and teosinte (reviewed in Doebley, 2004). eight or more rows around the ear (Fig. 1.1D). Parviglumis plants, when grown under the Teosinte kernels are very small (approximately short-day conditions typical of central Mex- one-tenth the weight of maize kernels) and ico, are bushy and comprised of many stalks are enclosed in a hardened fruitcase (Fig. 1.1E) (tillers) with long lateral branches ending in absent in modern maize (Fig. 1.1F). Teosinte male inflorescences (Fig. 1.1A). In contrast, ears shatter and disperse their seeds upon most modern maize plants are unbranched, maturation, a characteristic absent in maize. (A) (B) (C) (D) (E) (F) Fig. 1.1. Teosinte (A) and maize (B) differ greatly in terms of number of stalks and male and female inflorescences. Teosinte ears (C) contain 5–12 kernels without the familiar cob structure characteristic of maize (D). The small teosinte seeds (E) are enclosed in a hard fruitcase, while maize kernels (F) are naked and weigh approximately ten times more than those of teosinte. 0003169069.INDD 2 7/21/2017 6:20:31 AM Kernel Evolution: From Teosinte to Maize 3 It is something of a mystery how native thousand years of domestication and was an peoples of Mexico used teosinte prior to do- important part of the Native American diet. mestication. There were no large domesticated animals in North America at the time, so it is unlikely teosinte was a forage crop. Modern maize is used primarily for grain, 1.2.2 The master regulators and a natural assumption is that teosinte of domestication was used similarly. However, its hard fruitcase would be a formidable deterrent, along Beginning in the 1800s, there were various with the limited amount of food obtained hypotheses concerning the origin of corn from the small seeds. George Beadle de- that involved an extinct progenitor species, vised a method to create “teo-tortillas” us- teosinte, tripsacum, pod corn, corngrass, ing a primitive metate (grinding stone) and and combinations thereof. During the 1930s, a water-based method to float off the broken debates revolved around the extreme pheno- fruitcases. Beadle also proposed that na- typic differences between maize and teo- tives could have popped teosinte, similar to sinte. In an effort to understand inheritance modern popcorn (Beadle, 1939). Others of these differences, Beadle examined the have proposed Native Americans chewed phenotypes of over 50,000 F2 plants derived or sucked out sugars stored in the pithy teo- from a cross between maize and teosinte sinte stalks (Iltis, 2000) or created fermented (Beadle, 1972). He determined that approxi- beverages (Smalley and Blake, 2003). mately 1 in 500 plants looked like very teosinte-like, or very maize-like, with a ratio that suggested four or five genes control the main morphological differences between 1.2.1 Archeological evidence maize and teosinte. Indeed, Beadle’s calculation of a hand- The oldest archeological ear/cob samples ful of genes has been largely supported by are from 6200 years ago, originating in Guilá quantitative trait locus (QTL) mapping stud- Naquitz Cave in Oaxaca (Benz, 2001), and ies of morphological differences between 5500-year-old samples from the San Marcos maize and teosinte. In an F2 population de- Cave in the Tehuacán Valley in Puebla (Long rived from a cross of a maize landrace with a et al., 1989). Unfortunately, these samples more distantly related teosinte subspecies are too old to bear kernels, but they do show (Zea mays ssp. mexicana, hereafter mexicana), non-shattering cobs with two to four rows of six major QTLs (chromosomes 1–5) were naked (no fruitcase) kernels. The oldest ker- found to underlie key traits that differenti- nel samples, though not intact, include ate maize and teosinte: lateral branch length microfossils dated to 8700 years old and and inflorescence architecture, and second- found on grinding stones from the Xihua- ary sex traits such as the hard fruitcase and toxtla Shelter in Guerrero (Piperno et al., paired floral spikelets (Doebleyet al ., 1990). 2009). Analysis of starch grains found on The QTL analysis of a second F2 population these stones revealed maize was the pri- derived from a primitive landrace crossed mary species processed and included pop- with parviglumis revealed the same gen- corn and other hard/flinty kernel types. Se- omic regions, suggesting domestication from quence analysis of ancient DNA obtained teosinte to a primitive maize landrace could from 660–4405-year-old ear samples from be accomplished by modifying a few key New Mexico and Mexico indicated that al- genes or gene regions (Doebley and Stec, leles representative of modern maize were 1993). present 4400 years ago (Jaenicke-Després Since then, several QTL have been fine et al., 2003). So, it is clear primitive maize mapped and cloned, revealing the import- with morphologically distinct ears and ker- ance of transcription factors controlling key nels, though perhaps not quite resembling steps in domestication. The important regula- modern maize, was grown within a few tor of apical dominance, teosinte branched 1 0003169069.INDD 3 7/21/2017 6:20:31 AM 4 S.A. Flint-Garcia (tb1), is located on the long arm of chromo- 1.2.3 A thousand small effect genes some 1 (Doebley et al., 1995). The domesticated underlie domestication allele of this transcription factor contains a Hopscotch transposable element 63 kb up- While QTL studies are useful as a forward stream of the start codon (Studer et al., 2011) genetics approach to determine genomic re- that results in higher expression of a lateral gions underlying a phenotype, reverse gen- branch repressor (Doebley et al., 1997). Thus, etics approaches can be used to scan the maize represses growth of lateral branches, genome for signatures of selection that resulting in fewer tillers. Also on chromo- could result in a phenotype related to the some 1 (short arm) is a QTL controlling pro- domestication syndrome. Selection during lificacy: in teosinte, the long lateral branches domestication results in a reduction of nu- bear many ears, while the maize lateral cleotide diversity relative to the progenitor branch bears a single terminal ear. The QTL and an excess of rare variants as popula- controlling prolificacy was fine mapped to tions recover from selection, and can be grassy tillers 1, a homeodomain leucine zip- measured using a variety of population gen- per transcription factor (Wills et al., 2013) etic statistics. For example, an analysis of that was previously demonstrated to control sequence diversity of 21 genes on chromo- tillering (Whipple et al., 2011).

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