Computational Systems Biology

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Computational Systems Biology Flower development
Teemu Teeri 23.2. 2006
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Flower development in four parts

1. ABC and beyond
2. Induction of flowering
3. Meristems and prepatterns
4. Regulatory networks

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Part 1ABC and beyondHomeotic genes that
determine organ identity in flowers
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Arabidopsis
Stamen
Petal
Sepal
Carpel
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Homeotic mutants
Homeosis Something has been changed into the
likeness of something else Bateson 1894
Wilhelm Johannsen
William Bateson
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Homeotic mutants
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Homeotic mutants grow correct organs in wrong
places
Normal flower
A mutant
B mutant
C mutant
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ABC model for organ identity determination in
flowers
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ABC model for organ identity determination in
flowers
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The ABC model explains homeotic mutants in
flowers
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Mutant phenotypes in Arabidopsis
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Double mutantsin Arabidopsis
A- B-
B- C-
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Double mutantsin Arabidopsis
A- B-
B- C-
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ABC genes in Arabidopsis and snapdragon
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MADS domain family of transcription factors
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Expression domains of ABC MADS-box genes
correlate with their function
AGAMOUS
APETALA3
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MADS domain proteins bind DNA as dimers
g e n e
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The two B-function genes form an autoregulatory
loop
GLO
DEF
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ABC MADS-box genes are necessary for development
of flower organs
Are they sufficient?
No, expression of ABC genes in leaves does not
convert leaves into flower organs.
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Phylogeny
Among the ABC MADS-box genes, phylogenetic
position and genetic function correlate.
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Arabidopsis MADS-box genes AGL2, AGL4 and AGL9
group outside of the ABC genes in fylogeny. When
mutated, there is no change in flower phenotype.
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In a triple mutant for AGL2, AGL4 and AGL9, all
organs in the Arabidopsis flower develop into
sepals
W1
W2
W3
W4
Triple mutant
Wild type
Organs W1-W4
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AGL2, AGL4 and AGL9 were renamed to SEPALLATA1,
SEPALLATA2 and SEPALLATA3
W1
W2
W3
W4
Triple mutant
Wild type
Organs W1-W4
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The triple mutant resembles the double mutant
where B and C function genes are inactive
The SEPALLATA function (SEP1, SEP2 or SEP3) is
needed to fulfill both the B function and the C
function in Arabidospis.
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Quaternary complexes of MADS domain proteins
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The Quartet Model of flower development
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ABC and SEP MADS-box genes are necessary for
development of flower organs
Are they sufficient?
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Conversion of Arabidopsis leaves into petals
Rosette leaves
Cotyledons
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Scanning electron microscopy is used to define
organ identity
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Unifying principles of flower development

• ABC model
• Striking in its simplicity
• Applicable to a wide range of flowering plants
• Central role of LEAFY
• Necessary and sufficient to specify a meristem as
  floral
• Integrator of floral induction pathways
• Key activator of the ABC genes

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Part 2How do we get there?Induction of flowering
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Meristems and phase transitions
Inflorescence meristem
Vegetative meristem
Flower meristem
wt
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Multiple inductive pathways control the timing of
flowering

• Long-day photoperiod
• Gibberellins (GA)
• Vernalization
• Autonomous pathway

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Induction of flowering Multiple cues
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Induction of flowering Multiple cues
Multiple cues are integrated by FLC, SOC1, FT and
LFY
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Meristem identity genes

• Shoot meristem identity genes
• TERMINAL FLOWER 1 (TFL1)
• Floral meristem identity genes
• LEAFY (LFY)
• APETALA 1 (AP1)

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Snapdragon TFL1 gt CEN, LFY gt FLO
Inflorescence meristem
Flower meristem
CEN FLO
cen FLO
centroradialis mutant
wild type
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Meristem identity genes
Inflorescence meristem
Vegetative meristem
Flower meristem
wt
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TFL1 versus LFY and AP1
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Part 3Meristems and prepatternsHow ABC is laid
down?
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Meristems are stem cells of the plant
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Maintenance of the shoot apical meristem SAM
SAM
CLA3
WUS
WUS expression gives the meristem a prepattern
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Other prepatterns
UFO
UFO
UNUSUAL FLOWER ORGANS (UFO) patterns all meristems
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Other prepatterns
Floral SAM
Vegetative SAM
LEAFY
LEAFY marks the flower meristem
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WUS induces AGAG represses WUS
SAM
AG
WUS
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WUS induces AGAG represses WUS
SAM
AG
WUS
LEAFY
Unlike CLAVATA3, AGAMOUS expression is only
initially dependent on WUSCHEL
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WUS induces AGAG represses WUS
SAM
AG
LEAFY
Repression of the SAM organizer terminates the
meristem
Unlike CLAVATA3, AGAMOUS expression is only
initially dependent on WUSCHEL
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WUS induces AGAG represses WUS
SAM
ag
WUS
LEAFY
Failure in repression of the SAM organizer keeps
the meristem proliferating
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AP1 is initially expressed throughout the meristem
SAM
AP1
LEAFY
APETALA1 is induced by LEAFY
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AG represses AP1
SAM
AG
AP1
LEAFY
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B genes use the UFO prepattern
AP3
UFO
LEAFY
LEAFY and UFO induce AP3 expression in a region
where whors 2 and 3 (petals and stamens) will
develop
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B genes use the UFO prepattern
PI
PI is initially induced also in the center of the
flower meristem
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B genes use the UFO prepattern
PI
AP3PI
PI is initially induced also in the center of the
flower meristem
The B gene autoregulatory loop stabilizes B gene
expression
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Patterning ABC genes
SAM
AG
AP3PI
AP1
LEAFY
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A complete picture
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Part 4Regulatory networks
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Regulatory networks
Figure 2. Logical Rules for AP1, AP2, FUL, AP3,
and PI. The state of each network node
(rightmost column in each table) depends on the
combination of activity states of its input nodes
(all other columns in each table). X represents
any possible value. Comparative symbols (lt and gt)
are used when the relative values are important
to determine the state of activity of the target
node. AP1 (A), AP2 (B), FUL (C), AP3 (D), and PI
(E).
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Regulatory networks
Figure 4. Gene Network Architecture for the
Arabidopsis Floral Organ Fate Determination.
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Regulatory networks
The Steady States of the NetworkModel Coincide
with Experimental Gene Expression Profiles The
network had 139,968 possible initial conditions,
and it attained only 10 fixed-point attractors or
steady gene expression states (see supplemental
data online for complete basins of attraction).
These steady gene states (Table 1) predicted by
the model coincide with the gene expression
profiles that have been documented experimentally
in cells of wild-type Arabidopsis inflorescence
meristems and floral organ primordia. For
example, in the Infl steady states, floral
meristem identity genes (LFY, AP1, and AP2) and
floral organ identity genes (AP1, AP2, AP3, PI,
SEP, and AG) are off, whereas the inflorescence
identity genes (EMF1 and TFL1) are on.
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Reading

• Jack, T. 2004 Molecular and genetic mechanisms
  of floral control. Plant Cell 16, S1-S17.
• Espinosa-Soto et al. 2004 A gene regulatory
  network model Plant Cell 16
  2923-2939