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© 2015 American Society of Plant Biologists
STRIGOLACTONES
www.plantcell.org/cgi/doi/10.1105/tpc.109.tt0411
© 2015 American Society of Plant Biologists
Strigolactones contribute to a
devastating form of plant parasitism
Striga are parasitic
plants that are the
single largest biotic
cause of reduced crop
yields throughout Africa
(> $10 billion per year in
yield losses)
StrigaHost
Root
parasites
Striga germination is
induced by
strigolactones produced
by host plant roots Striga hermonthica
Image source: USDA APHIS PPQ Archive
© 2015 American Society of Plant Biologists
Strigolactones (SLs) regulate
seemingly unrelated events
Striga
Host
Root
AM fungi
SLs inhibit shoot
branching
SLs promote associations
with arbuscular mycorrhizal
(AM) fungi
SLs promote germination of
parasitic Striga plants
© 2015 American Society of Plant Biologists
Strigolactones inhibit shoot
branching
Image courtesy RIKEN
Wild type SL-deficient
In mutant plants unable to
make SLs, many more
shoot branches grow out
© 2015 American Society of Plant Biologists
Strigolactones promote beneficial
symbiotic interactions
Image courtesy of Mark Brundrett
Symbiotic AM fungi
SLs promotes the symbiotic association with AM
fungi. This symbiosis occurs in 80% of land plants
and helps them assimilate nutrients from the soil
Arbuscular is derived
from Latin for tree
(arbor). Mycorrhiza
means “fungus root”
© 2015 American Society of Plant Biologists
Strigolatones promote germination
of parasitic Striga seeds
Striga-infested maize field
Their common name is witchweed
because the plants appear to be cursed.
Typically Striga infestation causes
reductions in crop yields of 50 – 100%
Image source USDA APHIS PPQ Archive
© 2015 American Society of Plant Biologists
Image courtesy RIKEN
What is the
connection between:
•Shoot branching
•Root parasitism, and
•Root symbiosis?
© 2015 American Society of Plant Biologists
Three seemingly independent topics
converged on SLs
Evolution of plant
parasitism
Origins of plant /
mycorrhizal symbiosis
> 460 mya
Search for
branching factor...
1960s – 1970s
Purification and
characterization of
strigol from roots
1900s - Role of auxin in
shoot branching described
1990s – 2000s
Branching mutants
described in petunia, pea,
Arabidopsis and rice
2008:
Strigolactones
inhibit shoot
branching
1800s - Recognition of
AM fungus / plant
symbiosis
1800s - Host plant factor
required for parasitic seed
germination
2005:
Strigolactones
promote hyphal
branching
© 2015 American Society of Plant Biologists
Strigolactones have been co-opted
for various functions
O O
O OO
OH
SL’s ancestral
function may have
been communication
between individuals of
the same species (as
pheromones or
quormones)
AM fungi
Root parasite
O
O OO
H
O
SLs now contribute to communication within
an individual (as hormones), and between
individuals of different species (and
kingdoms) (as allelochemicals)
See for example Tsuchiya, Y. and McCourt, P. (2012). Strigolactones as small molecule communicators. Mol. BioSyst. 8: 464-469; Delaux, P.-M., et al., (2012). Origin of strigolactones in the green lineage. New
Phytol. 195: 857-871; Proust, H., et al., (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development. 138: 1531-1539.
© 2015 American Society of Plant Biologists
Lecture Outline
• Synthesis
• Perception and signaling
• Strigolactones in whole-
plant processes:
– Shoot branching
– Other developmental effects
– Moss colony growth
– Symbiosis
– Germination
• Towards the elimination of
Striga parasitism
Image source USDA APHIS PPQ Archive
© 2015 American Society of Plant Biologists
Synthesis and transport
In a search for stimulators of Striga
germination, strigolactones were purified
from cotton roots in 1966 and the
chemical structure determined in 1972
Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E., and Egley, G.H. (1966). Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant.
Science 154: 1189-1190; Reprinted with permission from Cook, C.E., Whichard, L.P., Wall, M., Egley, G.H., Coggon, P., Luhan, P.A., and McPhail, A.T. (1972).
Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J. Am. Chem. Soc. 94: 6198-6199.
© 2015 American Society of Plant Biologists
Strigolactones (SLs) are a small
family of compounds
Reprinted from Humphrey, A.J., and Beale, M.H. (2006). Strigol: Biogenesis and physiological activity. Phytochemistry 67: 636-640 with permission from Elsevier; See also Boyer, F.D., et al.. and
Rameau, C. (2012). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: 1524-1544.
5-Deoxystrigol
SYNTHESIS
There are many
naturally occurring
SLs, derived from
5-deoxystrigol
© 2015 American Society of Plant Biologists
The stimulator of Striga germination
derives from the carotenoid pathway
fluridone
MEP pathway
GGPP
phytoene
b-carotene
5-deoxystrigol
Carotenoid-
deficient
mutants do
not make
germination
stimulator
WT WT
mutant mutant
Through the use of maize mutants and
enzyme inhibitors, carotenoids were
demonstrated to be the precursors of SLs
Matusova, R., Rani, K., Verstappen, F.W.A., Franssen, M.C.R., Beale, M.H., and Bouwmeester, H.J. (2005). The strigolactone germination
stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 139: 920-934.
© 2015 American Society of Plant Biologists
Genes involved in SL biosynthesis
were identified by genetic methods
Reprinted from Booker, J., et al. (2004). MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14: 1232-1238
with permission from Elsevier; Morris, S.E., et al. (2001). Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 126:
1205-1213; Ishikawa, S., et al. (2005). Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46: 79-86 by permission of the Japanese Society of Plant
Physiologists. Simons, J.L., et al. (2007). Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol. 143: 697-706.
WT max3 WT rms5
Strigolactone-deficient
mutants in Arabidopsis,
pea, rice and petunia show
similar short, branchy
phenotypes
The MORE AXILLARY GROWTH3 (MAX3),
RAMOSUS5 (RMS5) , DWARF17 (D17) and
DECREASED APICAL DOMINANCE3 (DAD3)
genes all encode a carotenoid cleavage
dioxygenase (CCD7)
WT dad3
© 2015 American Society of Plant Biologists
SL biosynthesis pathway
carlactone
MAX3, D17, RMS5, DAD3:
MAX4, D10 ,RMS1, DAD1:
MAX1
STRIGOLACTONES
CCD7
CCD8
(P450)MAX; Arabidopsis
D; rice
RMS; pea
DAD; petunia
These
reactions occur
in the plastid
D27 (β-carotene-9-isomerase)
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi,
S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200.; Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. (2012) Recent advances
in strigolactone research: chemical and biological aspects. (in press). Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S.,
Bouwmeester, H., Beyer, P., and Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.
© 2015 American Society of Plant Biologists
D27 encodes an Fe-binding enzyme
necessary for SL synthesis
Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J. and Wang, Y. (2009). DWARF27, an iron-
containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell. 21: 1512-1525.
Wild-type
(Shiokari) d27
Strigolactones are detected in
exudates of wild-type but not d27 roots
Standard
Wild-type exudate
d27 exudate
The rice D27 is a β-
carotene-9-isomerase also
found in other plants
© 2015 American Society of Plant Biologists
Rice SL biosynthesis mutants are
rescued by exogenous SL
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K.,
Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200;
Control
2nd leaf tiller1st leaf tiller
1 c
m1 c
m
WT d10 d17
GR24(1 µM)
d10 and d17 are
rescued by
exogenous SL
(GR24 is a
synthetic SL)WT d10 d17
D17
D10
© 2015 American Society of Plant Biologists
WT max1 max3 max4
Control
GR24 (5 µM)
Arabidopsis SL biosynthesis mutants
are rescued by SL
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K.,
Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200; Seto Y,
Kameoka H, Yamaguchi S, Kyozuka J. (2012) Recent advances in strigolactone research: chemical and biological aspects. (in press).
MAX1
MAX4
MAX3
© 2015 American Society of Plant Biologists
MAX1 encodes a P450 enzyme
involved in shoot branching
Reprinted from Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to
produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449 with permission from Elsevier.
max1WT
MAX1 is
expressed
throughout the
plant, primarily
in association
with vascular
tissuesMAX1
© 2015 American Society of Plant Biologists
SL synthesis in root or shoot is
sufficient to control shoot branching
Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a
cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449.
max3
WT
max3 Scion
Root
WT
max3
WT
Grafts
Reciprocal grafts, in which wild-
type tissue is either the root or
scion, have normal phenotypes;
this says that the branch-
controlling signal can be made in
either tissue, and can move from
root to shoot
© 2015 American Society of Plant Biologists
Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream
of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449; Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer,
P., and Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.
An intermediate between MAX4 and
MAX1 action can move in the plant
max4
max1
max1
max4
MAX1
STRIGOLACTONES
MAX4
In this experiment mobile, graft-
transmissible intermediate in SL
synthesis is produced in max1
roots, and converted into SL in
max4 shoots
Carlactone is a good
candidate as the SL mobile
signalling molecule
© 2015 American Society of Plant Biologists
Kretzschmar, T., Kohlen, W., Sasse, J., Borghi, L., Schlegel, M., Bachelier, J.B., Reinhardt, D., Bours, R., Bouwmeester, H.J. and
Martinoia, E. (2012). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature. 483: 341-344.
WTdad1
(=max4)
PDR1 has been identified as a
strigolactone exporter
pdr1
SLs are present
in pdr1 root
extracts, but not
prd1 exudates,
supporting its
role as a
transporter
pdr1 mutants are
less colonized by
AM fungi, and
stimulate less
parasitic seed
germination
Loss-of-function pdr1 mutant show:
•increased shoot branching
•decreased exudation of SLs
•decreased symbiotic interactions
© 2015 American Society of Plant Biologists
The distribution of PDR1 is
consistent with its roles in transport
Reprinted from Sasse, J., Simon, S., Gübeli, C., Liu, G.-W., Cheng, X., Friml, J., Bouwmeester, H., Martinoia, E. and Borghi, L. (2015). Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional
strigolactone transport. Curr. Biol. 25: 647-655 and Ruyter-Spira, C., Al-Babili, S., van der Krol, S. and Bouwmeester, H. (2013). The biology of strigolactones. Trends Plant Sci. 18: 72-83 with permission from Elsevier.
SLs are transported
shootward and
outward from the root
© 2015 American Society of Plant Biologists
Synthesis and transport - summary
Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-
Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.
SLs are derived from
carotenoids;
Early steps occur in
the plastids of root
and shoot
carlactone
MAX3, RMS5, D17, DAD3
MAX4, RMS1, D10, DAD1
MAX1
STRIGOLACTONES
(CCD7)
(CCD8)
(P450)MAX; Arabidopsis
RMS; pea
D; rice
DAD; petunia
D27 (β-carotene-9-isomerase)
Carlactone is an SL
intermediate (and may
be a mobile signal)
© 2015 American Society of Plant Biologists
Perception and signaling
Reprinted by permission from Macmillan Publishers Ltd: Zhou, F., et al and Wan, J. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.
1. D14 is an α/β-
fold hydrolase that
binds SLs
2. D3 is an F-box protein that promotes
interaction with the proteasome
3. The interaction between SLs, D14
and D3 leads to degradation of target
proteins including D53 (SMAX)
© 2015 American Society of Plant Biologists
1. D14 is an α/β-fold hydrolase that
binds SLs ¥
Loss-of-function
d14 mutants are
SL insensitive
and show
increased shoot
branching; the
orthologous
gene in petunia
is dad2
Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S. and Kyozuka, J. (2009). d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 50:
1416-1424; Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching
hormone, strigolactone. Curr Biol. 22: 2032–2036
Genetic studies Biochemical
studies
D14 and DAD2
are α/β-fold
hydrolases
similar to the
GID1 protein
involved in
gibberellin
perception
© 2015 American Society of Plant Biologists
The α/β-fold hydrolase D14/DAD2
cleaves SL
Nakamura, H., Xue, Y.L., Miyakawa, T., Hou, F., Qin, H.M., Fukui, K., Shi, X., Ito, E., Ito, S., Park, S.H., Miyauchi, Y., Asano, A., Totsuka, N., Ueda, T., Tanokura, M., and Asami, T. (2013). Molecular mechanism of
strigolactone perception by DWARF14. Nat Commun. 4: 2613. Seto, Y., and Yamaguchi, S. (2014). Strigolactone biosynthesis and perception. Curr. Opin. Plant Biol. 21: 1-6 with permission from Elsevier.
Hydrolysis
© 2015 American Society of Plant Biologists
SL receptors D14/DAD2 are related
to the KAI2 karrikin receptors
Conn, C.E., Bythell-Douglas, R., Neumann, D., Yoshida, S., Whittington, B., Westwood, J.H., Shirasu, K., Bond, C.S., Dyer, K.A., and Nelson, D.C. (2015). Convergent evolution of
strigolactone perception enabled host detection in parasitic plants. Science 349: 540-543. Reprinted with permission from AAAS.
Karrikins are small
molecules present in
smoke that are
structurally similar to
SLs and can induce
seed germination
D14 probably arose from a duplication of KAI2
before the evolution of seed plants
© 2015 American Society of Plant Biologists
Parasitic Striga make highly-
sensitive SL receptors
From Toh, S., Holbrook-Smith, D., Stogios, P.J., Onopriyenko, O., Lumba, S., Tsuchiya, Y., Savchenko, A. and McCourt, P. (2015). Structure-
function analysis identifies highly sensitive strigolactone receptors in Striga. Science. 350: 203-207. Reprinted with permission from AAAS.
The SL receptor gene family
is amplified in StrigaShHTL7 encodes a highly
sensitive receptor protein
that confers germination
sensitivity to SLs in vivo
© 2015 American Society of Plant Biologists
2. D3, an F-box protein, promotes
interaction with the proteasome
GR24
(1 µM)
Control
d3WT
MAX2, D3 and
RMS4 encode F-box
proteins related to
those involved in
auxin and jasmonate
signaling
Auxin receptor
Jasmonate co-receptor
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new
terpenoid plant hormones. Nature 455: 195-200. Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogne, K., Beveridge, C.A., and Rameau, C. (2006). Branching genes are conserved across species. Genes
controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol. 142: 1014-1026.
© 2015 American Society of Plant Biologists
In the presence of SLs, DAD2/D14
interacts with D3/MAX2
Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perception
of the plant branching hormone, strigolactone. Curr Biol. 22: 2032–2036 ;Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A.,
Ghisalberti, E.L. and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 108: 8897-8902.
SL concentration-
dependent interaction
between DAD2 (D14)
and MAX2 (D3)
Pro
tein
inte
raction
Model of SL signal transduction
Note the similarity of this model with those for auxin,
jasmonate, salicylate and gibberellin signalling
A current model is that SLs promote the interaction
between DAD2/D14 receptor and MAX2/D3,
leading to degradation of a signaling repressor
(D3)
© 2015 American Society of Plant Biologists
Karrikin signals are transduced in a
similar manner as SLs
Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L. and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone
signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 108: 8897-8902.; Waters, M.T., Nelson, D.C., Scaffidi, A., Flematti, G.R., Sun, Y.K., Dixon, K.W. and Smith, S.M. (2012). Specialisation within
the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 139: 1285-1295.
By analogy to SLs, karrikin-
binding to KAI2 could promote its
interaction with MAX2 and the
degradation of repressor proteinsMAX2 is
needed for SL
and karrikin
signaling
© 2015 American Society of Plant Biologists
3. Genetic approaches identified
D53/SMXLs in SL signalling
Stanga, J.P., Smith, S.M., Briggs, W.R. and Nelson, D.C. (2013). SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163: 318-330.
Jiang, L., and Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405. Reprinted by permission from Macmillan Publishers Ltd: Zhou, F. et al.,, and Wan, J. (2013). D14-
SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.
SMAX = Suppressor of MAX2
Loss-of-function smax1
mutants suppress SL
mutant phenotypes
Gain-of-function dominant d53 mutants show
a SL-resistant, branchy phenotype
© 2015 American Society of Plant Biologists
Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., Wu, F., Mao, H., Dong, W., Gan, L., Ma, W., Gao, H., Chen, J., Yang, C., Wang, D., Tan, J., Zhang, X., Guo, X., Wang, J., Jiang, L., Liu, X., Chen, W., Chu,
J., Yan, C., Ueno, K., Ito, S., Asami, T., Cheng, Z., Wang, J., Lei, C., Zhai, H., Wu, C., Wang, H., Zheng, N., and Wan, J. (2013). Reprinted by permission from Macmillan Publishers Ltd: D14-SCFD3-dependent
degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.
The D53 protein is a SL signaling repressor. D53 degradation by the proteasome depends on
interaction with the D14/DAD2 receptor bound to SL.
D14-SL and D3/MAX2 intermediate interaction between the D53 repressor and the SCF complex.
In Arabidopsis, D14 degradation is induced by SL via a MAX2-dependent proteasome
mechanism.
Model: Strigolactone promotes D14-
SCFD3-mediated degradation of the
repressor D53
© 2015 American Society of Plant Biologists
Reprinted by permission from Macmillan Publishers Ltd: Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., Yi, W., Zhao, L., Ma, H., He, Y., Wu, Z., Melcher, K., Qian, Q.,
Xu, H.E., Wang, Y., and Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405
• D14/DAD2 is an a/b hydrolyze
that binds SL, allowing
interactions with the F-box
protein D3/MAX2
• D3/MAX2 brings the SCF
complex and E2 ubiquitin ligase
to D53 for polyubiquitination, and
further degradation by the
proteasome
• D53 degradation leads to
transcriptional activation of SL-
target genes
Signaling summary
© 2015 American Society of Plant Biologists
Strigolactones and whole-plant
processes
Seto, Y., Kameoka, H., Yamaguchi, S., and Kyozuka, J. (2012). Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol. 53: 1843-1853 by permission of Oxford University Press.
Strigolactones
have diverse
roles in the
development of
vascular plants
and moss
This include
positive and
negative effects
© 2015 American Society of Plant Biologists
Strigolactones regulate shoot /root
branching and nutrient responses
Reprinted from Brewer, P.B., Koltai, H., and Beveridge, C.A. (2013). Diverse roles of strigolactones in plant development. Mol Plant. 6: 18-28 with permission of Elsevier.
SL mutants
produce more
shoot and
root branches
In nutrient
deficiency,
elevated SLs
repress shoot
branching and
promote root
hair elongation
© 2015 American Society of Plant Biologists
Strigolactones dampen polar auxin
transport (PAT)
Reprinted from Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C., and Leyser, O. (2006). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr.
Biol. 16: 553-563 with permission from Elsevier; Crawford, S., Shinohara, N., Sieberer, T., Williamson, L., George, G., Hepworth, J., Müller, D., Domagalska, M.A., and Leyser, O. (2010).
Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913 reproduced with permission.
SL-deficient plants show
increased polar auxin transport
Transported
auxin
Auxin
+SL
PIN
In shoots, strigolactones
promote internalization of PIN
auxin efflux transporters,
decreasing polar auxin transport
© 2015 American Society of Plant Biologists
How do
strigolactones
inhibit bud
outgrowth?
Goulet, C. and Klee, H.J. (2010). Climbing the branches of the strigolactones pathway one discovery at a time. Plant Physiol. 154: 493-496.
© 2015 American Society of Plant Biologists
Axillary bud outgrowth is hormonally
and environmentally responsive
McSteen, P. (2009). Hormonal regulation of branching in grasses. Plant Physiol. 149: 46-55; Brewer, P.B., Dun, E.A., Ferguson, B.J., Rameau, C., and Beveridge,
C.A. (2009). Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol. 150: 482-493.
(Axillla means armpit)
bud• Auxin and SLs
inhibit outgrowth
• Cytokinins (CKs)
promote it
© 2015 American Society of Plant Biologists
SL effect on branching can occur via
effects on polar auxin transport
Shinohara, N., Taylor, C., and Leyser, O. (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474.
© 2015 American Society of Plant Biologists
SL effects on shoot branching can
also be auxin-independent
Brewer, P.B., Dun, E.A., Gui, R., Mason, M.G. and Beveridge, C.A. (2015). Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol. 168: 1820-1829.
Transcriptional targets of
SLs include BRC1, a
transcription factor that
represses bud outgrowth
© 2015 American Society of Plant Biologists
SLs in whole plant responses -
summary
Reprinted from Smith, Steven M. and Waters, Mark T. (2012). Strigolactones: Destruction-
dependent perception? Curr. Biol. 22: R924-R927, with permission from Elsevier.
SLs have pleiotropic
effects on plant
development, mediated
in part by auxin and
other hormones
© 2015 American Society of Plant Biologists
Strigolactones promote branching in
arbuscular mycorrhizal fungi
Reprinted by permission from Macmillan Publishers Ltd: Akiyama, K., Matsuzaki, K.-i., and Hayashi, H. (2005). Plant
sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827 copyright 2005.
SL
SL
SL
SL
Time Zero Time 24 hours
SLs promote
hyphal
branching
© 2015 American Society of Plant Biologists
When AM fungi perceive SLs, they
initiate symbiosis with the host plant
Reprinted by permission from Macmillan Publishers Ltd: Parniske, M. (2008) Arbuscular mycorrhiza: the
mother of plant root endosymbiosis. Nat. Rev. Microbiol. 6: 763 – 775 copyright 2008.
© 2015 American Society of Plant Biologists
Both partners benefit from the
symbiosisThe fungus gets sugars
produced by photosynthesis
The plant gets
nitrogen and
phosphorus
from the soil
by way of the
symbiotic
fungal
association
The arbuscule
provides a large
surface area for
nutrient
exchange
© 2015 American Society of Plant Biologists
0 500 1000 1500 2000 25005-deoxystrigol (pg/plant/5 days)
Low Mg
Low Ca
Low K
Low P
Low N
control
SL levels are elevated in sorghum
root exudates under low P and N
Courtesy of K. Yoneyama and adapted from Yoneyama, K., Xie, X., Kusumoto, D., Sekimoto, H., Sugimoto, Y., Takeuchi, Y., and Yoneyama, K. (2007). Nitrogen deficiency as well as phosphorus
deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227: 125-132.
© 2015 American Society of Plant Biologists
–P+P
AM fungi
In nutrient-poor soils:
•SL synthesis increases
•Shoot branching decreases and
root branching increases
•AM symbiosis increases
These responses
enhance plant
survival under low
nutrient conditions
© 2015 American Society of Plant Biologists
Strigolactones promote germination
in parasitic and other plants
Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K.,
Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200 Dörr, I. (1997). How
Striga parasitizes its host: a TEM and SEM study. Annals of Botany. 79: 463-472, by permission of Oxford University Press;
O O
O OO
OH
Strigolactones were first
characterized as
inducers of Striga
germination (1960s)
© 2015 American Society of Plant Biologists
Striga species (witchweeds) are
serious agricultural pests
•Major cereal crops are infested: corn, sorghum, millet and rice
•70 million hectares are infested
•Food productions for 300 million people are affected
•Financial loss is estimated to be approximately 10 billion USD
•No effective control measure has been developed
Adapted from Ejeta, G. and Gressel, J. (eds) (2007) Integrating new technologies for striga control: towards
ending the witch-hunt. World Scientific Publishing, Singapore; Image sources: USDA APHIS PPQ Archive,
Florida Division of Plant Industry Archive, Dept Agriculture and Consumer Services.
Witchweed infestation
HeavyModerateLight
Striga asiatica
Striga hermonthica
© 2015 American Society of Plant Biologists
How can we move towards Striga-
resistant crops?
Agricultural practices:
•Field treatments
•Allelopathic approaches
Genetic approaches:
•Modify SL structure:
encrypt the signal
•Suppress branching in SL-
deficient plants
Image courtesy of International Institute of Tropical Agriculture (IITA)
© 2015 American Society of Plant Biologists
Orobanche (broomrape)-infested
carrot field
Photo credit Shmuel Golan courtesy of Yaakov Goldwasser
© 2015 American Society of Plant Biologists
Striga
asiatica
Image courtesy of Prof. Julie Scholes & Mamadou Cissoko
Rice field
infested
with Striga
© 2015 American Society of Plant Biologists
Parasitic plants infect
60% of farmlands in
sub-Saharan Africa
Image source USDA APHIS PPQ Archive
© 2015 American Society of Plant Biologists
Agricultural practices can reduce
crop losses from Striga
Photo courtesy Ken Hammond (USDA)
• Before planting, apply germination
stimulants to promote “suicidal
germination” (no host = no survival)
• Apply fertilizers to reduce SL
production by crop plants.
• These methods are prohibitively
expensive in many parts of the
developing world.
© 2015 American Society of Plant Biologists
Intercropping with beneficial plants
can reduce Striga infestation
Maize intercropped with Desmodium uncinatum
Desmodium is a nitrogen-fixing
legume that enriches the soil, and
also produces allelopathic chemicals
that interfere with Striga parasitism
Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. and Woodcock, C.M. (2008). Integrated pest management: the push–pull approach for controlling insect pests and
weeds of cereals, and its potential for other agricultural systems including animal husbandry. Phil. Trans. R. Soc. B 363: 611-621 copyright 2008 The Royal Society.
Desmodium uncinatum
© 2015 American Society of Plant Biologists
Do all SLs promote Striga
germination and affect branching?
5-Deoxystrigol Orobanchol 2’-epi-orobanchol
Sorgomol SolanacolOrobachyl acetate
Strigyl acetateStrigolSorgolactone
Fabacyl acetate7-oxoorobanchyl
acetateOrobanchyl acetate
A BC
D
There are many
different naturally
occurring SLs –
how does their
structure affect
their function?
© 2015 American Society of Plant Biologists
Saturated (3,6'-dihydro-) GR24 isomers
do not induce Striga germination
O
O OO
O O
O OO
O O
O OO
O O
O OO
O
Isomer I Isomer II Isomer III Isomer IV
GR24
Enol etherO O
O OO
Isomers of saturated GR24
© 2015 American Society of Plant Biologists
…but an isomer of saturated GR24
promotes interactions with AM fungi
Adapted from Akiyama, K., Ogasawara, H., Ito, S. and Hayashi, H. (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol., 51: 1104-1117 see also Boyer, F.D., de Saint
Germain, A., Pillot, J.P., Pouvreau, J.B., Chen, V.X., Ramos, S., Stevenin, A., Simier, P., Delavault, P., Beau, J.M. and Rameau, C. (2012). Structure-activity relationship studies of strigolactone-related molecules for
branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: 1524-1544.
Can we make synthetic SLs with beneficial but not
detrimental effects? YES
Can we engineer plants to make these? MAYBE
AM
fungi Striga
+++ –O
O OO
O
Saturated
GR24
O O
O OO
+++ +++GR24
© 2015 American Society of Plant Biologists
Can we engineer Striga resistance?
Rice d10 SL-deficient mutant...
(1) Parasitism
(2) Symbiosis
Root parasite
(3) Shoot branching
O
O OO
H
O
O O
O OO
(1) No germination of Striga
seeds around the root
(2) Reduced AM fungi symbiosis
(but not fully inhibited)(3) Too many shoot branches
Are these effects separable?
AM fungi
© 2015 American Society of Plant Biologists
Can we engineer Striga resistance?
Rice d10 SL-deficient mutant...
(1) Parasitism
(2) Symbiosis
Root parasite
(3) Shoot branching
O
O OO
H
O
O O
O OO
Modify downstream component
(e.g. d10 suppressor mutants)
Can we normalize shoot branching
in SL-deficient mutants?
These experiments are in progress
with a goal to producing Striga-
resistant plants
(1) No germination of Striga
seeds around the root
(2) Reduced AM fungi symbiosis
(but not fully inhibited)(3) Too many shoot branches
AM fungi
© 2015 American Society of Plant Biologists
Summary (1) Perception and
signaling
de Saint Germain, A., Bonhomme, S., Boyer, F.D., and Rameau, C. (2013). Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol. 16: 583-589.
© 2015 American Society of Plant Biologists
Conclusions and future directions
AM fungi
O
O OO
H
O
O O
O OO
Strigolactones are synthesized in roots of
nutrient-limited plants
SLs enhance AM fungi symbiosis
SLs repress shoot branching and
adventitious root formation
SLs stimulate primary root growth, root hair
elongation, secondary growth, and leaf
senescence
© 2015 American Society of Plant Biologists
AM fungi
O
O OO
H
O
O O
O OO
Conclusions and future directions
How do SLs integrate with other hormones
and signals to control shoot, root branching
and leaf senescence?
Can we modify the SL biosynthesis pathway
to alter the types and activities of SLs
produced?
What are the evolutionary origins and
ancestral functions of SLs?
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