Transcript Domestication genes in plants

PLANT OF THE DAY: Marshelder
•Close relative of ragweed and sunflower
•Domesticated in eastern North America as an oilseed
•Domesticated form now extinct
Marshelder (Iva)
Crop domestication
Big Questions
•Why were plants domesticated?
•Where were plants domesticated?
•When were plants domesticated?
•How quickly were they domesticated?
•What were the selection pressures that caused
domestication?
•What kinds of genetic changes are under selection during
domestication?
•Do analyses of evolution under domestication inform us
about evolution under natural selection?
•Why haven’t any major crops been domesticated recently?
Centres of Plant Domestication
• Concept first devised by Vavilov in 1919
• Archaeological evidence suggests that hunter-gatherers independently
began cultivating food plants in at least 11 regions of the world (Doebley et
al. 2006)
Domestication
‘Domestication is the process by which humans
actively interfere with and direct crop evolution.’
• It involves a genetic bottleneck:
• Often only few genes are actively selected and account
for large shifts in phenotype.
• Crops exhibit various levels of domestication.
What is a domestication syndrome?
A domestication syndrome describes the properties
that distinguish a certain crop from it’s wild progenitor.
Typically such characteristics are:
• larger fruits or grains
• more robust plants
• more determinate growth / increased apical
dominance
• loss of natural seed disperal
• fewer fruits or grains
• decrease in bitter substances in edible structures
• changes in photoperiod sensitivity
• synchronized flowering
Tomato - Fewer and Larger Fruits
Sunflowers - reduced branching, larger seeds,
increased seed set per head
Wheat - reduced seed shattering, increased seed size
Squash – larger, fleshier fruits
Corn – reduced fruitcase, softer glume, more kernels
per cob, no dispersal, reduced branching, apical
dominance
Lettuce – leaf size/shape, fewer secondary compounds
Rice – no shattering,
larger grains
Domestication is a process
• The distinction ‘domesticated’ or ‘not domesticated’ is an oversimplification
• Some crops have moved further along this process further than
others.
• We can recognize different levels of domestication
• How can we decide which level?
• Different domestication traits were selected for progressively
•Distinction between selection under domestication vs. crop
diversification  more targeted, ‘conscious’ selection during
diversification
• ‘Slow’ rate of evolution of different domestication traits
despite faster rates suggested by models
• Artificial selection can be “similar across different taxa,
geographical origins and time periods”
• Parallel evolution for “sticky glutinous varieties” in rice and
foxtail millets, all through selection at the waxy locus
• Most QTL studies suggest that many domestication traits are
controlled by a few genes of large effect – not though in
sunflower
• Population genomic studies in maize suggest 2 – 4% of genes
show evidence of artificial selection
Domestication of Maize
How often has maize been domesticated?
– Sampling (Matsuoka et al, 2002)
How often has maize been domesticated?
– Once. (Matsuoka et al, 2002)
Tracking footprints of maize domestication and evidence for a
massive selective sweep on chromosome 10
(Tian et al., 2009 PNAS)
Teosinte branched 1 (tb1)
• was identified as a major QTL controlling the difference in apical
dominance between maize and its progenitor, teosinte (Doebley et al.,
1997; Doebley, 2004)
• is a member of the TCP family of transcriptional regulators, a class of
genes involved in the transcriptional regulation of cell-cycle genes.
•Differences in tb1 expression patterns between maize and teosinte indicate
that human selection was targeted at regulatory differences that produced a
higher level of tb1 message in maize.
• Lack of any fixed amino acid differences between maize and teosinte in
the TB1 protein supports this hypothesis.
•First domestication gene cloned.
“For maize tb1 … [the selection coefficient] is in the range 0.05
to 0.2, comparable to cases of natural selection.” (Purugannan
and Fuller, 2009)
Teosinte glume architecture1 (tga1)
• was identified as a QTL controlling the formation of the casing that
surrounds the kernels of the maize ancestor, teosinte (Wang et al., 2005)
• is a member of the squamosa-promoter binding protein (SBP) family of
transcriptional regulators.
• tga1 has phenotypic effects on diverse traits including cell lignification,
silica deposition in cells, three-dimensional organ growth, and organ size
•The difference in function between the maize and teosinte alleles of tga1
appears to be the result of a single amino acid change. The fact that there
are no discernable differences in gene expression supports this
interpretation.
Flowering Locus T (FT)
Flowering Locus T (FT) protein is main
component of florigen
Four flowering time gene homologs – all members of the FT gene family –
experienced selective sweeps during a stage of sunflower domestication
Elite
Landrace
Wild
Reduced nucleotide diversity (π) in HaFT paralogs with
early domestication or improvement
Genetics 2011; 187:271-287
Genetic and functional analyses identify causative mutations in HaFT paralogs
Domesticated Allele of HaFT1
has frameshift mutation
Current Biology 2010; 20:629-635
Loss of function mutation at FT also
contributes to heterosis in other species
“already kicking ass
in commercial
tomato production.”
D. Zamir, Dec. 11, 2012,
Asilomar
Krieger et al. 2010
Homozygote
(sFT)
Heterozygote (sft Homozygote (sft)
X sFT)
Nature Genetics 42, 459-465, (2010)
b
Floret
number
80
a
40
0.0
a
Homozygote Heterozygote Homozygote
Domesticated
Wild
(frameshift)
(in-frame)
Seed weight (g)
Heterozygotes with frameshift allele exhibit
heterosis
2.0
b
a
1.0
0.0
a
Homozygote Heterozygote Homozygote
Domesticated
Wild
(frameshift)
(in-frame)
Current Biology 2010; 20:629-635
Domestication genes in plants
FT
Sunflower Transcriptional regulator; flowering time
Yes
Yes
frameshift
mutation
Crop Diversification genes in plants
The genetic basis of the evolution of non-shattering
Non-shattering is often regarded as the hallmark of
domestication in most seed crops because it renders a
plant species primarily dependent on humans for survival
and propagation:
• rice gene sh4 (similar to the genes encoding MYBlike transcription factors in maize)
• rice quantitative trait locus (QTL) qSH1, which
encodes a homeobox-containing protein
• the wheat gene Q, which is similar to genes of the
AP2 family in other plants
• In sunflower likely controlled by multiple genes
Domestication genes in plants
• Maize and rice domestication seem to suggest few loci of
large effect are important
• Sunflower domestication seems to suggest many loci of small
to intermediate effect are important
• 9 domestication genes in plants so far, as well as 26 other loci
known to underlie crop diversity
• Of the 9 domestication loci, 8 encode transcriptional
activators.
•
More than half of crop diversification genes encode enzymes.
 Domestication seems to be associated with changes in
transcriptional regulatory networks, whereas crop
diversification involves a larger proportion of enzymeencoding loci (lots of them loss-of-function alleles).
The role of polyploidy in domestication
Where does the cultivated gene pool come from?
Sclerotinia resistance locus
Wild Introgressions
H. petiolaris
H. argophyllus
H. annuus
landraces
Unanswered questions
Why is there a disagreement between archeobotanical and
molecular data regarding the speed of domestication?
Why are some crops only weakly domesticated?
Are the major effect domestication genes/mutations cloned
so far representative of other crops/genes/mutations?
What is the role of reproductive isolation in domestication?
Do domesticated plants carry high levels of genetic load?