1. Computational Systems Biology
Flower development
Teemu Teeri
Flower development

2. Flower development in four parts
ABC and beyond
Induction of flowering
Meristems and prepatterns
Regulatory networks
Flower development

3. Part 1 ABC and beyond Homeotic genes that determine organ identity in flowers
Flower development

4. Arabidopsis
Stamen
Petal
Sepal
Carpel
Flower development

5. Homeotic mutants Homeosis:
‘Something has been changed into the likeness of something else’
Bateson 1894
Johannsen: terms ’gene’, ’genotype’, ’phenotype’,...
Bateson: terms ’homeosis’, ’genetics’,...
Wilhelm
Johannsen
William
Bateson
Flower development

6. Homeotic mutants
Flower development

7. Homeotic mutants grow correct organs in wrong places
Normal flower
A mutant
B mutant
C mutant
Flower development

8. ABC model for organ identity determination in flowers
sepal
petal
stamen
carpel
Flower development

9. ABC model for organ identity determination in flowers
Flower development

10. The ABC model explains homeotic mutants in flowers
sepal
petal
stamen
carpel B C
carpel
stamen B A
sepal
petal A C
sepal
carpel
Flower development

11. Mutant phenotypes in ArabidopsisC
sepal
petal
stamen
carpel B C
carpel
stamen B A
sepal
petal A C
sepal
carpel
Flower development

12. Double mutants in ArabidopsisC
carpel
B- C- A
sepal
Flower development

13. Double mutants in Arabidopsis
A- B- C-
leaf B A C C
carpel
B- C- A
sepal
Flower development

14. ABC genes in Arabidopsis and snapdragon
Flower development

15. MADS domain family of transcription factorsK
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
Flower development

16. Expression domains of ABC MADS-box genes correlate with their function
AGAMOUS
APETALA3
Flower development

17. MADS domain proteins bind DNA as dimers
transcription
g e n e
Flower development

18. The two B-function genes form an autoregulatory loop
globosa
DEF
GLO
deficiens
DEF
GLO
GLO
DEF
DEF
GLO
Flower development

19. ABC MADS-box genes are necessary for development of flower organs
leaf B A C
Are they sufficient?
No, expression of ABC genes in leaves does not convert leaves into flower organs.
Flower development

20. Phylogeny
Among the ABC MADS-box genes, phylogenetic position and genetic function correlate.
sepal
petal
anther
carpel B A C
Flower development

21. When mutated, there is no change in flower phenotype.
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.
Flower development

22. In a triple mutant for AGL2, AGL4 and AGL9, all organs in the Arabidopsis flower develop into sepals
Wild type
Triple mutant
Organs W1-W4
Flower development

23. AGL2, AGL4 and AGL9 were renamed to SEPALLATA1, SEPALLATA2 and SEPALLATA3
Wild type
Triple mutant
Organs W1-W4
Flower development

24. 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. A
sepal
B- C-
Flower development

25. Quaternary complexes of MADS domain proteins
Flower development

26. The Quartet Model of flower development
Flower development

27. ABC and SEP MADS-box genes are necessary for development of flower organs
leaf B A C
Are they sufficient?
Flower development

28. Conversion of Arabidopsis leaves into petals
Rosette leaves
Cotyledons
Flower development

29. Scanning electron microscopy is used to define organ identity
Flower development

30. 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 B A C
sepal
petal
stamen
carpel
Flower development

31. Part 2 How do we get there? Induction of flowering
Flower development

32. Meristems and phase transitionsCO
FLC
AGL20
AGL24
LFY/FLO
Vegetative
meristem
Inflorescence
meristem
Flower
meristem wt
Flower development

33. Multiple inductive pathways control the timing of flowering
Long-day photoperiod
Gibberellins (GA)
Vernalization
Autonomous pathway
Flower development

34. Induction of flowering
Multiple cues
Figure 1 Plants integrate multiple cues during the switch to flowering. In Arabidopsis input signals influencing the transition are light (photoperiod and quality), ambient temperature, phytohormones and long periods of cold temperature (vernalization). Additionally, floral repressors antagonize the activity of promotive cues.
Flower development

35. Induction of flowering
Multiple cues
Multiple cues are integrated by FLC, SOC1, FT and LFY
Flower development

36. Meristem identity genes
Shoot meristem identity genes
TERMINAL FLOWER 1 (TFL1)
Floral meristem identity genes
LEAFY (LFY)
APETALA 1 (AP1)
Flower development

37. Snapdragon TFL1 –> CEN, LFY –> FLO
Inflorescence
meristem
Flower
meristem
CEN
FLO
cen
FLO
centroradialis
mutant
wild type
Flower development

38. Meristem identity genes
Vegetative
meristem
Inflorescence
meristem
Flower
meristem
TFL1
LEAFY
TFL1
LFY wt
Flower development

39. TFL1 versus LFY and AP1 35S-TFL1 35S-LFY 35S-AP1 LFY ↓ AP1 ↓ TFL1 ↓
Flower development

40. Part 3 Meristems and prepatterns How ABC is laid down?
Flower development

41. Meristems are stem cells of the plant
Flower development

42. Maintenance of the shoot apical meristem SAM
WUS
CLA3
CLAVATA3 expression is dependent on WUSCHEL
 Stable feedback loop that maintains the size of SAM
SAM
CLA3
WUS
WUS expression gives the meristem a prepattern
Flower development

43. UNUSUAL FLOWER ORGANS (UFO) patterns all meristems
Other prepatterns
UFO
UFO
UNUSUAL FLOWER ORGANS (UFO) patterns all meristems
Flower development

44. LEAFY marks the flower meristem
Other prepatterns
Floral
SAM
Vegetative
SAM
LEAFY
LEAFY marks the flower meristem
Flower development

45. WUS induces AG AG represses WUS
SAM
A wus mutant flower: central organs are missing AG
WUS
Flower development

46. WUS induces AG AG represses WUS
SAM
A wus mutant flower: central organs are missing AG
WUS +
LEAFY
Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL
Flower development

47. WUS induces AG AG represses WUS
SAM AG
LEAFY
Repression of the SAM organizer terminates the meristem
Unlike CLAVATA3, AGAMOUS expression is only initially dependent on WUSCHEL
Flower development

48. WUS induces AG AG represses WUS
SAM ag
WUS +
LEAFY
Failure in repression of the SAM organizer keeps the meristem proliferating
Flower development

49. AP1 is initially expressed throughout the meristem
SAM
AP1
LEAFY
APETALA1 is induced by LEAFY
Flower development

50. AG represses AP1
SAM AG B A C
AP1
LEAFY
Flower development

51. 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
Flower development

52. B genes use the UFO prepattern
AP3
PI AP3 PI
The B gene autoregulatory loop
stabilizes B gene expression PI
PI is initially induced also in the center of the flower meristem
Flower development

53. B genes use the UFO prepatternPI
AP3+PI
PI is initially induced also in the center of the flower meristem
The B gene autoregulatory loop
stabilizes B gene expression
PI AP3
AP3 PI
Flower development

54. Patterning ABC genes SAM sepal petal stamen carpel B A C AG AP3+PI AP1
LEAFY B A C
sepal
petal
stamen
carpel
Flower development

55. A complete picture…
Flower development

56. Part 4 Regulatory networks
Flower development

57. 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).
Flower development

58. Regulatory networks
Figure 4. Gene Network Architecture for the Arabidopsis Floral Organ
Fate Determination.
Flower development

59. 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.
Flower development

60. 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:
Flower development