23.2. 2006 Flower development 1 Computational Systems Biology Flower development Teemu Teeri 23.2. 2006

23.2. 2006 Flower development 1

Computational Systems Biology

Flower development

Teemu Teeri23.2. 2006


Flower development in

four parts1. ABC and beyond

2. Induction of flowering

3. Meristems and prepatterns

4. Regulatory networks


Part 1ABC and beyond

Homeotic genes that determine organ identity in flowers


Sepal

Petal

Carpel

Stamen

Arabidopsis


Homeotic mutants

WilhelmJohannsen

William Bateson

Homeosis:‘Something has been changed into the likeness of something else’

Bateson 1894


Homeotic mutants


Normal flower A mutant

B mutant C mutant

Homeotic mutants grow correct organs in wrong

places


BA C

sepa

lpe

tal

stam

enca

rpel

ABC model for organ identity determination in flowers


ABC model for organ identity determination in flowers


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


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


A

sepa

lse

pal

sepa

lse

pal

C

carp

el

carp

el

carp

el

carp

el

A- B-

B- C-

Double mutantsin Arabidopsis


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


Arabidopsis Snapdragon A function

APETALA1 APETALA2

SQUAMOSA

B function

PISTILLATA APETALA3

GLOBOSA DEFICIENS

C function

AGAMOUS

PLENA

ABC genes in Arabidopsis and snapdragon


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


AGAMOUS APETALA3

Expression domains of ABC MADS-box genes correlate

with their function


MADS domain proteins bind DNA as dimers

g e n e

M2M1

M2M1

transcription


The two B-function genes form an autoregulatory

loop

globosa

DEFGLO

DEFGLO

deficiens

DEFGLO

DEFGLO


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


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


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.


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


Wild type Organs W1-W4Triple mutant

W1

W2

W3

W4

AGL2, AGL4 and AGL9 were renamed to SEPALLATA1,

SEPALLATA2 and SEPALLATA3


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


Quaternary complexes of MADS domain proteins


The Quartet Model of flower development


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


Rosette leaves Cotyledons

Conversion of Arabidopsis leaves into petals


Scanning electron microscopy is used to define

organ identity


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


Part 2How do we get there?

Induction of flowering


Inflorescencemeristem

Vegetative meristem

Flowermeristem

COFLC

AGL20AGL24 LFY/FLO

wt

Meristems and phase transitions


Multiple inductive pathways control the timing of flowering

• Long-day photoperiod

• Gibberellins (GA)

• Vernalization

• Autonomous pathway


Induction of floweringMultiple cues

http://arjournals.annualreviews.org/na101/home/literatum/ar/journals/production/genet/2003/37/1/annurev.genet.37.110801.142640/images/large/ge37_0371_1.jpeg


Multiple cues are integrated by FLC, SOC1, FT and LFY

Induction of floweringMultiple cues


Meristem identity genes

• Shoot meristem identity genes– TERMINAL FLOWER 1 (TFL1)

• Floral meristem identity genes– LEAFY (LFY)– APETALA 1 (AP1)


wild type

centroradialismutant

Snapdragon TFL1 –> CEN, LFY –> FLO

Inflorescencemeristem Flower

meristemCEN

FLO

cen

FLO


Meristem identity genes

Inflorescencemeristem

Vegetative meristem

Flowermeristem

wt

TFL1

LEAFY

TFL1

LFY


TFL1 versus LFY and AP1

35S-LFY35S-AP1

35S-TFL1LFY ↓AP1 ↓ TFL1 ↓


Part 3Meristems and prepatterns

How ABC is laid down?


Meristems are stem

cells of the plant


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


Other prepatterns

UFO

UFO

UNUSUAL FLOWER ORGANS (UFO) patterns all meristems


Other prepatterns

LEAFY marks the flower meristem

LEAFY

FloralSAM

VegetativeSAM


WUS induces AGAG represses WUS

WUS

AG

SAM

A wus mutant flower: central organs are missing



WUS

AG

SAM

A wus mutant flower: central organs are missing

+LEAFY

Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL



AG

SAM

LEAFY

Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL

Repression of the SAM organizer terminates the

meristem



WUS

ag

SAM

+LEAFY

Failure in repression of the SAM organizer keeps

the meristem proliferating


AP1 is initially expressed throughout

the meristemSAM

LEAFY

APETALA1 is induced by LEAFY

AP1


AG represses AP1

AG

SAM

LEAFY

AP1

BA C


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



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



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


Patterning ABC genes

SAM

LEAFY

AP1

AP3+PI

AG

BA C

sepa

lpe

tal

stam

enca

rpel


A complete picture…


Part 4Regulatory networks


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).


Regulatory networks

Figure 4. Gene Network Architecture for the Arabidopsis Floral OrganFate Determination.


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.


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

Documents

23.2. 2006 Flower development 1 Computational Systems Biology Flower development Teemu Teeri 23.2. 2006