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Review
Ten thousand years ago human societies around the globe began to transition from
hunting and gathering to agriculture. By 4000 years ago, ancient peoples had completed
the domestication of all major crop species upon which human survival is dependent,
including rice, wheat, and maize. Recent research has begun to reveal the genes respon-
sible for this agricultural revolution. The list of genes to date tentatively suggests that
diverse plant developmental pathways were the targets of Neolithic “genetic tinkering,”
and we are now closer to understanding how plant development was redirected to meet
the needs of a hungry world.
Most members of our modern industrial societies have human needs. For many crops, domestication has ren-
never seen and would not recognize the unpromising wild dered the plant completely dependent on humans such
plants that are the progenitors of our remarkably produc- that it is no longer capable of propagating itself in nature.
tive crops. Very few members of these societies would Maize and cauliflower are good examples of such highly
survive if all they had were a field of wild grain and herbs modified forms. However, other crops, such as hemp,
and their own wits to sustain them. Yet, 10,000 years ago, carrot, and lettuce, have been more modestly modified
people who could not read, write, or do calculus pros- compared to their progenitors, and they can either revert
pered on diets composed of wild plants and animals. to the wild or become self-propagating weeds.
Even more remarkably, these ancient peoples began a There is a common suite of traits—known as the
plant-breeding program that transformed hundreds of “domestication syndrome”—that distinguishes most
wild plant species into domesticated crops, including all seed and fruit crops from their progenitors (Hammer,
of the most highly productive crops—rice, wheat, maize— 1984). Compared to their progenitors, food crops typi-
on which human survival is dependent today. cally have larger fruits or grains, more robust plants
In this review, we first summarize some basic observa- overall, more determinate growth or increased api-
tions about domestication and the origin of agriculture. cal dominance (the robust growth of the central stem
How were crops modified during domestication? What in comparison to the side stems), and a loss of natu-
was the breeding process by which wild species were ral seed dispersal so that seeds remain attached to the
converted to crops? And when and where did domesti- plant for easy harvest by humans (Figure 1). Remarkably,
cation take place? Next, we discuss the genes that have crops often have fewer (although larger) fruits or grains
been identified to date as controlling key differences in per plant than their progenitors. A variety of physiologi-
plant structures and physiology that distinguish crops cal changes are also involved. These include a loss of
and their progenitors or different crop varieties from one seed dormancy, a decrease in bitter substances in edi-
another. We then discuss how population genetic analy- ble structures, changes in photoperiod sensitivity, and
ses can be used to discover genes that were the targets synchronized flowering.
of selection during plant domestication by humans. We
end by summarizing what has been learned about how The Domestication Process
domestication modified plant development to produce Most researchers believe that agriculture began as an
today’s crops and by giving some examples of how this attempt to modify the landscape and thereby encour-
knowledge is being exploited to drive crop improve- age the growth of edible wild plants at the expense of
ments in ways not possible using traditional plant breed- less useful ones (Smith, 1998). Among hunter-gather-
ing methods. ers such as the Australian Aborigines, burning of native
vegetation was practiced because species of grasses
The Domestication Syndrome favored as food thrived after the burning. From such a
Plant domestication is the genetic modification of a wild practice, it is a small step to burning an area devoid of
species to create a new form of a plant altered to meet useful plants and then sowing seed of favored species
DNA studies of archaeological maize from northeast The archaeological record of the domestication and
Mexico and the southwest United States have shown early history of other major crop plants, such as rice
that it is possible to track human selection for specific (Oryza sativa), remains incomplete. The earliest evidence
attributes that are not observable in the archaeological for domesticated rice has been recovered from the set-
record (Jaenicke-Despres et al., 2003). This highlights tlements of already sophisticated rice-farming societies
the potential for combining genetic and archaeological along the middle and lower Yangtze River corridor in
research in order to reconstruct the evolution of crop southern China. At the village settlement of Ho-mu-tu
plants spanning thousands of years. In similar fashion, along the lower Yangtze River, for example, 1 m thick
the recent genetic data tracing the temporal and geo- deposits of domesticated rice husks dating to about
graphical radiation of maize from southern Mexico to 7000 BP were recovered (Smith, 1998). These settle-
the limits of cultivation in the Americas compare very ments predate any sign of rice cultivation elsewhere in
closely to large scale efforts by archaeologists to track East Asia by several thousand years. As recently devel-
the gradual expansion of maize cultivation throughout oped methods of plant recovery and analysis are more
the Americas (Matsuoka et al., 2002; Blake, 2006). widely applied to earlier sites along the Yangtze and
Einkorn wheat (Triticum monococcum) provides a throughout East Asia, the initial domestication of rice will
similar, if less robust, example of cross illumination quite likely be pushed back in time another 1000–2000
from genetic and archaeological research on the initial years or more. Unfortunately, archaeological rice grains
domestication of major crop plants. A genetic com- cannot yet be assigned with any degree of confidence to
parison of modern domesticated and wild einkorn particular varieties (e.g., indica and japonica) on the basis
populations across the Fertile Crescent identified the of morphology. As a result, any better understanding of
Karacadağ mountain region of southeastern Turkey the initial domestication and early history of indica ver-
as its likely heartland of domestication (Heun et al., sus japonica will probably be based on genetic analysis
1997). Situated only about 200 km to the south, along of ancient and present-day populations of domesticated
the Euphrates River, the archaeological site of Abu and wild rice. For example, a recent analysis of DNA-
Hureyra has yielded the earliest evidence (9600 BP) sequence data has confirmed that indica and japonica
not only for domesticated einkorn wheat but also for are the products of separate domestication events, the
emmer wheat (Triticum araraticum) and barley (Hor- former south of the Himalaya and the latter in southern
deum vulgare) (Smith, 1998). The subsequent radia- China (Londo et al., 2006).
tion of these crop plants across the Fertile Crescent Another crop that has been the recent subject of
and then north and west throughout Europe has been landmark genetic research is the tomato (Lycopersicon
documented in some detail in the archaeological esculentum). Unfortunately, this crop is much less well
record of the two regions (Harris, 1996). documented in the archaeological record. Given the
cell death or the release of hydrolytic enzymes that dis- have been discovered as QTL, whereas others segre-
solve the bonds between cells in the abscission layer gate as Mendelian loci. For morphological and struc-
that separates the grain from the plant. tural traits, there are several excellent examples. Grain
qSH1 is another major QTL controlling shattering in number differences between rice varieties are control-
rice that has recently been cloned and shown to encode led by grain number1 (gn1), which encodes an oxidase/
a homeobox containing transcription factor (Konishi dehydrogenase that degrades the plant hormone cyto-
et al., 2006). By a combination of genetic approaches, kinin (Ashikari et al., 2005). Regulatory changes in some
Konishi and colleagues were able to demonstrate that alleles and a premature stop codon in another allele
a single nucleotide change in a cis-regulatory element both contribute to functional variation at gn1. In tomato,
of qSH1 obliterated expression of the cells that form the the difference between varieties with pear-shaped ver-
shattering zone, thus preventing shattering. qSH1 was sus round fruits is controlled by ovate, a novel regula-
first identified in a segregating population from japonica tory gene with a putative nuclear localization signal and
x indica cross, indicating that it differentiates these two homology to human Von Willebrand factor genes (Liu et
subspecies and suggesting that the loss of shatter- al., 2002). The functional polymorphism appears to be
ing involved independent genetic changes during their an early stop codon that conditions the pear shape. In
domestications. cole crops (Brassica oleracea), the BoCAL gene (a mem-
Although we have only a small sample of domestica- ber of the MADS box family of transcriptional regulators)
tion genes for major domestication traits, it is notable appears to be involved in the unusual inflorescence mor-
that none of the six domestication genes discussed phologies of broccoli and cauliflower, possibly due to an
above resulted from a null or loss-of-function mutation. early stop codon (Smith and King, 2000; Purugganan et
In three cases, regulatory changes are inferred, in one al., 2000).
an amino acid substitution is found, and in two cases The list of known genes contributing to physiologi-
there are combined regulatory and protein changes. cal or biochemical differences between crop varieties is
Also, it is notable that five of the six are transcription much longer (Table 1). Here are a few well-characterized
factors and the fifth a likely cellular signaling (regulatory) examples. Mendel’s wrinkled seed gene (r), which con-
gene. A longer list is needed before firm conclusions can verts the field pea into the garden pea, is the result of an
be drawn, though we expect transcriptional regulators Ac/Ds-like transposon insertion that disrupts the coding
will continue to be over-represented among the major sequence of a starch-branching enzyme (Bhattacha-
genes controlling morphological differences between ryya et al., 1990). In maize, yellow1 (y1) encodes a kernel
crops and their progenitors. specific phytoene synthase that produces yellow kernels
with high levels of carotenoids, a precursor for vitamin A
Genes Controlling Varietal Differences synthesis (Palaisa et al., 2003). The functional difference
In addition to genes controlling classic domestication appears to involve a change in promoter sequences
traits, many genes controlling differences between vari- such that y1, which is normally expressed in leaves, is
eties of a single crop or important agronomic traits have expressed in developing kernels. When it was discov-
been clearly identified (Table 1). Some of these genes ered that yellow corn provides improved nutrition for
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