Gibberellins were identified as
fungal compounds that promote
stem elongation
Bakanae disease
(Gibberella fujikuroi)
Bakanae disease means
“foolish seedling”, because
infected plants elongate too
rapidly, and are unable to
Uninfected support themselves; they
are also male sterile.
plant
Infected,
hyperelongated
plants
A Gibberellin (GA3)
Photo source: Nigel Cattlin, Visuals Unlimited, Inc.
© 2014 American Society of Plant Biologists
Later, gibberellins were identified as
endogenous plant growth regulators
Gibberellins promote stem
elongation and seed
germination. In some plants
they promote flowering and fruit
development
Wild-type pea
Mendel’s short peas
are deficient in GA
synthesis
Some plants are treated with GAsynthesis inhibitors to maintain a
shorter stature and prevent
lodging (tipping over)
Development
of many
seedless fruits
requires GA
application
Lester, D.R., Ross, J.J., Davies, P.J., and Reid, J.B. (1997) Mendel's stem length gene (Le) encodes a gibberellin 3[beta]-hydroxylase. Plant
Cell 9: 1435-1443; Wheat mage courtesy of Mary Burrows, Montana State University, Bugwood.org; Clementine photo by Azcolvin429.
© 2014 American Society of Plant Biologists
GA has been described as “an
inhibitor of an inhibitor”
A car doesn’t roll down a
hill when the brake is on
to inhibit it. Releasing the
brake “inhibits the
inhibitor”, allowing
another force (gravity) to
move it
GA doesn’t promote
growth on its own, but
instead inhibits growth
inhibitors (i.e. releases
the brakes)
© 2014 American Society of Plant Biologists
GA synthesis and homeostasis
In 1956, B.O. Phinney
found that some dwarf
mutants of Zea mays
could be rescued by
GA application
Wild type
Wild type
+ GA
dwarf-1
dwarf-1
+ GA
The pathway of GA biosynthesis
in plants was determined in part
by analysis of GA-deficient
dwarfs; an early use of the
“chemical genetics” approach
Phinney, B.O. (1956). Growth response of single-gene dwarf mutants in maize to gibberellic acid. Proc. Natl. Acad. Sci. USA 42: 185-189.
© 2014 American Society of Plant Biologists
The GA biosynthetic pathway is
complex
Stage 3 - cytoplasm
Stage 1 - proplastid
Active
GAs
Stage 2 - endomembranes
Hedden, P., Proebsting, W.M. (1999) Genetic analysis of gibberellin biosynthesis. Plant Physiol. 119: 365-370; Helliwell, C.A., Chandler,
P.M., Poole, A., Dennis, E.S., and Peacock, W.J. (2001). The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of
the gibberellin biosynthesis pathway. Proc. Natl. Acad. Sci. USA 98: 2065-2070, Copyright 2001 National Academy of Sciences USA.
© 2014 American Society of Plant Biologists
GA biosynthesis and deactivation
are tightly controlled
Auxin upregulates
GA synthesis.
Auxin
Temperature
and light
regulate
GA3ox
Active GAs
downregulate GA
synthesis and
upregulate GA
deactivation
Most genes are
expressed in a
cell-specific
manner
Thomas, S.G., Phillips, A.L., and Hedden, P. (1999). Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional
enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. USA 96: 4698-4703 Copyright 1999 National Academy of Sciences, USA.
© 2014 American Society of Plant Biologists
GA responses
Biosynthesis mutant
Response mutant
No GA signaling
Response mutant
Constitutive GA
signaling
Harberd, N.P., Belfield, E., and Yasumura, Y. (2009). The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism:
How an “inhibitor of an inhibitor" enables flexible response to fluctuating environments. Plant Cell 21: 1328-1339.
© 2014 American Society of Plant Biologists
GIBBERELLIN INSENSITIVE DWARF1
(GID1) encodes a GA receptor
Unlike biosynthesis
mutants, the rice gid1
mutant is not rescued by
GA – it is gibberellininsensitive
WT
gid1-1
Reprinted by permission from Macmillan Publishers, Ltd: NATURE. Ueguchi-Tanaka, M., et al. (2005) GIBBERELLIN
INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698, copyright 2005.
© 2014 American Society of Plant Biologists
When it binds GA, the receptor GID1
binds to DELLA proteins
“DELLA” refers to a
conserved amino acid
sequence at the N-terminus:
Asp-Glu-Leu-Leu-Ala
D- E- L -L - A
Reprinted by permission from Macmillan Publishers, Ltd: Nature. Murase, K., Hirano, Y., Sun, T.-p., and Hakoshima, T. (2008). Gibberellin-induced
DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463, Copyright 2008; Reprinted from Sun, T.-p. (2011). The molecular mechanism
and evolution of the GA GID1 DELLA signaling module in plants. Curr. Biol. 21: R338-R345 with permission from Elsevier.
© 2014 American Society of Plant Biologists
DELLAs complexed with GID1 are
recognized by an F-box protein
An F-box protein is a component of a
an SCF E3 ubiquitin ligase that
targets proteins for proteolysis
R
G
A
S
Reprinted from Sun, T.-p. (2011). The molecular mechanism and evolution of the GA GID1
DELLA signaling module in plants. Curr. Biol. 21: R338-R345 with permission from Elsevier.
© 2014 American Society of Plant Biologists
GAs repress photomorphogenesis
and DELLAs promote it
GA is required for etiolation
• Etiolation is a dark-growth
response that includes
elongated shoot growth and
unopened leaves
• The GA-deficient pea na mutant
does not show this normal dark
growth pattern, but can be
rescued with exogenous GA
Wild type
GA deficient
Alabadi, D., Gil, J., Blazquez, M.A., and Garcia-Martinez, J.L. (2004). Gibberellins
repress photomorphogenesis in darkness. Plant Physiol. 134: 1050-1057.
© 2014 American Society of Plant Biologists
The PIF3 and PIF4 transcription
factors are necessary for etiolation
PIF3/4
PIF3 and PIF4
activate the
transcription of
growthpromoting
genes, leading to
elongation of the
hypocotyl in the
dark
PIF3/4
DELLA
DELLA proteins
bind PIF3 and
PIF4 and
interfere with
their action
Reprinted from Davière, J.-M., de Lucas, M., and Prat, S. (2008) Transcription factor interaction: a central
step in DELLA function. Curr. Opin. Genet. Devel. 18: 295–303.with permission from Elsevier
© 2014 American Society of Plant Biologists
GA promotes DELLA degradation,
allowing PIF3 and PIF4 to act
GA
DELLA
PIF3/4
Reprinted from Davière, J.-M., de Lucas, M., and Prat, S. (2008) Transcription factor interaction: a central
step in DELLA function. Curr. Opin. Genet. Devel. 18: 295–303.with permission from Elsevier
© 2014 American Society of Plant Biologists
These studies reveal that DELLAs
can affect growth through their
actions on other proteins
PIF3/4
DELLA
DELLA
+ GA
PIF3/4
Other studies support the model that DELLA
act through transcriptional changes
Reprinted from Davière, J.-M., de Lucas, M., and Prat, S. (2008) Transcription factor interaction: a central
step in DELLA function. Curr. Opin. Genet. Devel. 18: 295–303.with permission from Elsevier
© 2014 American Society of Plant Biologists
GAs’ roles in whole-plant physiology
•GAs control growth and elongation by cell expansion and
cell division
•GAs mediate stress responses through DELLA proteins
•GAs promote seed germination and reserve mobilization
•GAs promote flowering
•GAs and DELLAs are central in many signaling schemes
© 2014 American Society of Plant Biologists
GAs promote growth through cell
expansion and division
GAs induce
expression of cellcycle regulatory
proteins called cyclins
Cell
expansion
Cell
division
Cell
expansion
GAs promote elongation
by cell wall loosening and
stabilizing the orientation
of cortical microtubules,
which help direct growth
© 2014 American Society of Plant Biologists
GAs promote elongation and
submergence avoidance in rice
Control
As water levels rise during
seasonal flooding, GA promotes
rapid stem elongation to keep the
top of the plant above the water line
Submerged
Two days of
submergence
induces tremendous
internode elongation
Kende, H., van der Knaap, E., and Cho, H.-T. (1998). Deepwater rice: A model plant to study stem elongation. Plant Physiol. 118: 1105-1110.
© 2014 American Society of Plant Biologists
Sometimes it is best to limit growth
under stressful conditions
Slow water rise –
avoid submergence
by GA-induced
growth
Control
Sub1A
Flooding
Rapid water rise
– conserve
energy by DELLAmediated growthinhibition
Rice that carry
the Sub1A gene
can survive
flooding by not
growing
Control
Sub1A
Fukao, T. and Bailey-Serres , J. (2008). Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of
gibberellin responses in rice. Proc Natl Acad Sci USA 105: 16814-16819 Copyright © 2008 by the National Academy of Sciences.
© 2014 American Society of Plant Biologists
Growth and environmental stress:
DELLAs integrate diverse signals
Submergence
Sub1A
Salt stress
Ethylene
Cold stress
DELLA function
Survival via decreased growth
© 2014 American Society of Plant Biologists
GA and ABA act antagonistically in
the control of seed germination
ABA promotes
desiccation tolerance
and dormancy
Seed germination requires
elimination of ABA and
production of GA to
promote growth and
breakdown of seed storage
products
Germination
Reserve
mobilization
Cell
expansion
GA
ABA
© 2014 American Society of Plant Biologists
During germination, GA induces
expression of nutrient-mobilizing
enzymes
Breakdown of starch in the
endosperm is initiated by GA
produced by the embryo or added
during the malting process
GA
GA
amylase
BARLEY
sugars
starch
Embryo
Endosperm
Aleurone
Images by Prof. Dr. Otto Wilhelm Thomé Flora von Deutschland, Österreich und der Schweiz 1885 and Chrisdesign.
© 2014 American Society of Plant Biologists
In some plants, GAs contribute to
the control of flowering
Flower promoting
signals
Flower inhibiting
signals
Photoperiod
GA
Ethylene
Stress
DELLA proteins
Samolus parviflorus,
a long-day plant,
grown in short-days
without or with
gibberellin treatment
Control
Gibberellin
In some plants that
require long days for
flowering, GA can
promote flowering
even in short days
© 2014 American Society of Plant Biologists
GAs and DELLAs
are central in many
signaling schemes
PD, protein degradation;
PPI, protein–protein
interaction;
TC, transcription
Reprinted from Sun, T.-p. (2011). The molecular mechanism and evolution of the GA GID1 DELLA
signaling module in plants. Curr. Biol. 21: R338-R345 with permission from Elsevier.
© 2014 American Society of Plant Biologists
Summary of GA action
Other
inputs
Synthesis
Pool of
bioactive GAs
Pool of
DELLAs
Deactivation
The biological
functions of GA are
mediated primarily
through their effects
on DELLA proteins
DELLA protein
functions include
the control of
transcription factor
activity
DELLA proteins are
also controlled by
other inputs including
light, biotic and
abiotic stresses and
other hormones
© 2014 American Society of Plant Biologists