23.2. 2006 flower development 1 computational systems biology flower development teemu teeri 23.2....
TRANSCRIPT
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23.2. 2006 Flower development 1
Computational Systems Biology
Flower development
Teemu Teeri23.2. 2006
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23.2. 2006 Flower development 2
Flower development in
four parts1. ABC and beyond
2. Induction of flowering
3. Meristems and prepatterns
4. Regulatory networks
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Part 1ABC and beyond
Homeotic genes that determine organ identity in flowers
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Sepal
Petal
Carpel
Stamen
Arabidopsis
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Homeotic mutants
WilhelmJohannsen
William Bateson
Homeosis:‘Something has been changed into the likeness of something else’
Bateson 1894
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Homeotic mutants
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Normal flower A mutant
B mutant C mutant
Homeotic mutants grow correct organs in wrong
places
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BA C
sepa
lpe
tal
stam
enca
rpel
ABC model for organ identity determination in flowers
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ABC model for organ identity determination in flowers
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BA C
sepa
lpe
tal
stam
enca
rpel
BC
carp
elst
amen
stam
enca
rpel
A C
sepa
lse
pal
carp
elca
rpel
BA
sepa
lpe
tal
peta
lse
pal
The ABC model explains homeotic mutants in flowers
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BA C
sepa
lpe
tal
stam
enca
rpel
A C
sepa
lse
pal
carp
elca
rpel
BC
carp
elst
amen
stam
enca
rpel
BA
sepa
lpe
tal
peta
lse
pal
Mutant phenotypes in Arabidopsis
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A
sepa
lse
pal
sepa
lse
pal
C
carp
el
carp
el
carp
el
carp
el
A- B-
B- C-
Double mutantsin Arabidopsis
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A
sepa
lse
pal
sepa
lse
pal
C
carp
el
carp
el
carp
el
carp
el
A- B-
B- C-
A- B- C-
leafleaf
leaf
leaf
BA C
Double mutantsin Arabidopsis
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Arabidopsis Snapdragon A function
APETALA1 APETALA2
SQUAMOSA
B function
PISTILLATA APETALA3
GLOBOSA DEFICIENS
C function
AGAMOUS
PLENA
ABC genes in Arabidopsis and snapdragon
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MADSN CI K
MADS
I
K
C
N
56 aa, highly conserved, DNA-binding, dimerisation
27-42 aa, considerable sequence variability
70 aa, moderately conserved, keratin related, protein-protein interactions
Poor or no sequence conservation
A region present in AG and related MADS proteins
MADS domain family of transcription factors
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AGAMOUS APETALA3
Expression domains of ABC MADS-box genes correlate
with their function
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MADS domain proteins bind DNA as dimers
g e n e
M2M1
M2M1
transcription
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The two B-function genes form an autoregulatory
loop
globosa
DEFGLO
DEFGLO
deficiens
DEFGLO
DEFGLO
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A- B- C-le
afleaf
leaf
leaf
BA C
Are they sufficient?
No, expression of ABC genes in leaves does not convert leaves into flower organs.
ABC MADS-box genes are necessary for development of
flower organs
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sepal
petal
anthercarpel
BA C
sepa
l
peta
lan
ther
carp
el
Among the ABC MADS-box genes, phylogenetic position and genetic function correlate.
Phylogeny
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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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Wild type Organs W1-W4Triple mutant
W1
W2
W3
W4
In a triple mutant for AGL2, AGL4 and AGL9, all organs in the
Arabidopsis flower develop into sepals
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Wild type Organs W1-W4Triple mutant
W1
W2
W3
W4
AGL2, AGL4 and AGL9 were renamed to SEPALLATA1,
SEPALLATA2 and SEPALLATA3
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A
sepa
lse
pal
sepa
lse
pal
B- C- The SEPALLATA function (SEP1, SEP2 or SEP3) is needed to fulfill both the B function and the C function in Arabidospis.
The triple mutant resembles the double mutant where B and
C function genes are inactive
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Quaternary complexes of MADS domain proteins
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The Quartet Model of flower development
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A- B- C-le
afleaf
leaf
leaf
BA C
Are they sufficient?
ABC and SEP MADS-box genes are necessary for development of flower
organs
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Rosette leaves Cotyledons
Conversion of Arabidopsis leaves into petals
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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
BA C
sepa
lpe
tal
stam
enca
rpel
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Part 2How do we get there?
Induction of flowering
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Inflorescencemeristem
Vegetative meristem
Flowermeristem
COFLC
AGL20AGL24 LFY/FLO
wt
Meristems and phase transitions
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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 floweringMultiple cues
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Multiple cues are integrated by FLC, SOC1, FT and LFY
Induction of floweringMultiple cues
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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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wild type
centroradialismutant
Snapdragon TFL1 –> CEN, LFY –> FLO
Inflorescencemeristem Flower
meristemCEN
FLO
cen
FLO
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Meristem identity genes
Inflorescencemeristem
Vegetative meristem
Flowermeristem
wt
TFL1
LEAFY
TFL1
LFY
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TFL1 versus LFY and AP1
35S-LFY35S-AP1
35S-TFL1LFY ↓AP1 ↓ TFL1 ↓
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Part 3Meristems and prepatterns
How 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
WUS
CLA3
SAM
WUS
CLA3
CLAVATA3 expression is dependent on WUSCHEL
Stable feedback loop that maintains the size of SAM
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
LEAFY marks the flower meristem
LEAFY
FloralSAM
VegetativeSAM
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WUS induces AGAG represses WUS
WUS
AG
SAM
A wus mutant flower: central organs are missing
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WUS induces AGAG represses WUS
WUS
AG
SAM
A wus mutant flower: central organs are missing
+LEAFY
Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL
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WUS induces AGAG represses WUS
AG
SAM
LEAFY
Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL
Repression of the SAM organizer terminates the
meristem
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WUS induces AGAG represses WUS
WUS
ag
SAM
+LEAFY
Failure in repression of the SAM organizer keeps
the meristem proliferating
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AP1 is initially expressed throughout
the meristemSAM
LEAFY
APETALA1 is induced by LEAFY
AP1
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AG represses AP1
AG
SAM
LEAFY
AP1
BA C
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B genes use the UFO prepattern
UFO
+LEAFY
AP3
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 is initially induced also in the center of the flower
meristem
PI AP3
PI AP3
AP3PI
The B gene autoregulatory loopstabilizes B gene expression
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B genes use the UFO prepattern
PI is initially induced also in the center of the flower
meristem
PI AP3+PI
PI AP3
AP3PI
The B gene autoregulatory loopstabilizes B gene expression
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Patterning ABC genes
SAM
LEAFY
AP1
AP3+PI
AG
BA C
sepa
lpe
tal
stam
enca
rpel
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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 (< and >) 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 OrganFate 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