Novel insights into strigolactone distribution and signalling - IJPB - Inra

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Novel insights into strigolactone distribution and signallingAlexandre de Saint Germain1, Sandrine Bonhomme1,Francois-Didier Boyer1,2 and Catherine Rameau1

Available online at www.sciencedirect.com

Strigolactones (SLs), a group of small carotenoid-derived

molecules, were first known for their function in the rhizosphere

in both symbiotic and parasitic interactions. Most of the

progress for deciphering SL biosynthesis and signalling

pathways comes from the use of high branching mutants

identified in several species demonstrating that SLs also play a

hormonal role in plant development. How SLs are perceived by

the different organisms on which they show bioactivity is a

current major challenge for the growing SL research

community. These molecules very likely predate the

colonization of land by plants and represent a fascinating

example of signalling molecules involved in key innovations

during plant evolution.

Addresses1 Institut Jean-Pierre Bourgin, INRA UMR1318 INRA-AgroParisTech,

F-78000 Versailles, France2 Centre de Recherche de Gif, Institut de Chimie des Substances

Naturelles, UPR2301 CNRS, F-91198 Gif-sur-Yvette, France

Corresponding author: Rameau, Catherine

([email protected])

Current Opinion in Plant Biology 2013, 16:xx–yy

This review comes from a themed issue on Cell signalling and gene

regulation 2013

Edited by Caren Chang and John Bowman

1369-5266X/$ – see front matter, # 2013 Elsevier Ltd. All rights

reserved.

http://dx.doi.org/10.1016/j.pbi.2013.06.007

IntroductionSL research has increased markedly since their discovery

as a plant hormone in 2008 for their role in inhibiting

shoot branching [1,2]. During the last five years, novel

hormonal functions have been demonstrated [3], a likely

receptor has been identified [4��] and important progress

has been made in deciphering the biosynthesis pathway

from carotenoids with the identification of the intermedi-

ate carlactone ([5��] and Figure 1). SLs exuded by the

host root stimulate hyphal growth of the obligate bio-

trophic arbuscular mycorrhizal (AM) fungi [6]. Arbuscular

mycorrhizal symbiosis occurring in more than 80% of land

plants, should play in the future a determinant role in

agriculture to reduce abiotic stresses. Later during evol-

ution, the obligate parasitic plants, Striga (witchweeds)

and Orobanche (broomrapes), causing devastating yield

reductions in several major crops, used SLs to develop a

Please cite this article in press as: de Saint Germain A, et al.: Novel insights into strigolactone distr

www.sciencedirect.com

system inducing seed germination only when seeds were

in close proximity to the host root [7]. Consequently

current research on these interkingdom signalling mol-

ecules will have a significant impact on both fundamental

and applied perspectives.

In this review, structural diversity of natural SLs will be

examined and structural requirements for SL bioactivity

for the three major functions (hormonal, symbiotic and

parasitic interactions) will be compared. Current knowl-

edge of SL reception for branching control will be pre-

sented with the first report on structural data to determine

how SLs interact with the receptor. Recent studies on the

origin of SLs during plant evolution will be given and

hypotheses on alternative SL biosynthesis and signalling

pathways discussed.

Diversity of SLs and bioactivity in differentmodelsThe structural core of SLs is a tricyclic lactone (ABC rings)

with various substitution patterns on AB rings. It is con-

nected via an enol ether bridge to an invariable a,b-

unsaturated furanone moiety (D-ring). To date, at least

19 naturally occurring SLs (Figure 2aI and aII) have been

identified and characterized in root exudates of various

land plants [7,8]. They can be separated into two families

according to a recent structure revision [9�], that is, one in

which the stereochemistry in the BCD part is the same as

(+)-strigol, and the other in which the stereochemistry in

the BCD part is the same as (�)-orobanchol. The roles of

SL stereochemistry and their various chemical decorations

need to be determined in the future. The recent discovery

of the intermediate carlactone (Figure 2aIII) [5��], was a

major breakthrough in understanding the SL biosynthesis,

suggesting that the BC rings are formed after the D ring to

give 5-deoxystrigol via putative(s) cytochrome P450

enzyme(s), possibly MAX1 (Figure 1). Further hydroxyl-

ations, epoxidation/oxidation and methyl transfers or

acetylation would lead to hydroxy-SLs or acetylated-SLs.

The SL community continues to develop SL analogues

[10–12] that are easily accessible in sizeable quantities,

and more stable facilitating structure–activity relationship

(SAR) studies in different models (Figure 2bI, bII and

bIII). The bioactiphore for the germination of parasitic

weed seeds, extensively studied in the past, was found to

reside in the CD part [12]. Essential structural features for

AM fungi appear to be similar, but important SL structure

variations seem to affect bioactivity such as the presence

of the ABC-rings, reported as essential for AM fungi but

ibution and signalling, Curr Opin Plant Biol (2013), http://dx.doi.org/10.1016/j.pbi.2013.06.007

Current Opinion in Plant Biology 2013, 16:1–7


[email protected]


http://www.sciencedirect.com/science/journal/13695266

2 Cell signalling and gene regulation 2013


Figure 1

all-trans-β -carotene

Isomerase (AtD27, PsD27, D27 )

9-cis-β-carotene

CCD7 (MAX3 , RMS5 , D17 /HTD1, DAD3 )

β-apo-10′-carotenal

carlacton e

CCD8 (MAX 4,RMS1 , D10 , DAD1)

CYP45 0 (MAX 1, 2 PsMAX1 , 5 O sMAX1 , Ph MAX 1)

strigo lacton es?

Physiolog icaleffect

F-bo x protein (MAX 2, RMS4, D3, Ph MAX2 A-B)

TCP transc ription factor (BRC 1, PsBRC 1, FC1)

α/β Hydrolase (AtD14, D14 , DAD2 )

Bio

syn

thes

isP

erce

pti

on

/S

ign

allin

g

MAX Ara bidop sis

RMS Pea

D Rice

DAD Petunia

Current Opinion in Plant Biology

Schematic representation of the SL biosynthesis and signalling pathway for the control of shoot branching with genes so far identified in the four model

species (boxed).

not for parasitic seeds and for branching (Figure 2b) [13–15]. Few studies have been described for the hormonal

function of SLs [1,2,15,16]. Through an SAR study in pea,

we established that the presence of a Michael acceptor

and a methylbutenolide or a dimethylbutenolide motif in

the same molecule is essential [17�]. We demonstrated

that SLs show potent activity for the control of shoot

branching in a structure dependent manner but with low

specificity [17�,18]. The differences in bioactivity

observed in the different systems suggest that they use

distinct modes of perception. Biochemical and structural

studies with proteins belonging to the a/b-hydrolase

superfamily have started to provide insights into SL

reception for its function on shoot architecture.

SL reception, a novel mechanism among planthormones?Studies of branching mutants and analogy with other

plant hormone receptors indicated that the F-box protein

MAX2 from Arabidopsis and the a/b-hydrolase D14 from

rice [19] were good candidates for the SL receptor [20].

D14 protein was also a possible activating enzyme to

transform SL into a bioactive molecule. Characterization

of DAD2, the petunia orthologue of D14, showed that this

a/b-hydrolase presented both enzymatic and receptor

activities and suggested a novel mechanism-of-action of

SL on its target protein [4��,21]. X-ray crystallography

studies of DAD2, AtD14 and OsD14 [22,23�] confirmed

that they belong to the a/b hydrolase fold family. Their

structure forms a hydrophobic pocket containing the

conserved Ser–His–Asp catalytic triad (Figure 3a). The

interaction between the protein and the synthetic SL



GR24 was confirmed by differential scanning fluorimetry

(DSF) for DAD2 [4��] and by isothermal titration calori-

metry (ITC) for OsD14 [23�]. Surprisingly, the binding of

GR24 to the DAD2 protein destabilized it, whereas

conventional hormone binding to its receptor stabilizes

the protein. In a yeast two-hybrid assay, GR24 was shown

to trigger an interaction between DAD2 and the petunia

F-box protein, PhMAX2A [4��]. The structure of D14 is

very similar to that of the gibberellins (GA) GID1 re-

ceptor. GID1 undergoes a conformational change when

GAs bind to it, resulting in closure of the N-terminal lid

over the binding pocket and interaction of the lid with the

GA negative regulator DELLA [25]. For SL, the function

of the lid appears different, with higher conformational

stability in D14, even in the absence of ligand [24].

D14 exhibits weak binding affinity for GR24, low for a

receptor (Kd = 0.36 mM vs. 5 mM for gibberellin A4 with

OsGID1) [22,25] indicating that a co-factor or a co-re-

ceptor may be involved for increasing binding affinity. In

addition to binding SLs, both DAD2 and OsD14 catalyze

hydrolysis of GR24, however with slow enzymatic activity

[4��].

In vitro studies showed that both rice and Arabidopsis D14

hydrolysed the GR24 into ABC-ring and D-ring products

[23�] (Figure 3b); in petunia, neither of the two hydrolytic

products, the ABC-ring product and an unidentified com-

pound retained any SL activity [4��].

Most, if not all, SLs have been identified in root exudates

and extracts. Studies for SL identification in shoot tissue




Evolution of strigolactone signalling de Saint Germain et al. 3


Figure 2

©Le Tacon / INR A ©Rameau / INR A

O O

X OO

A BC

D

Stereochemistryis not important

ABC-rings canbe replaced byan aromatic ring

Substitutions at C3' position in D-ring are tolerated

R

3′

O O

X OO

A BC

D

Stereochemistryis important

A-ring modificationshardly affect activity

R

O O

O OO

A BC

D


A-ring modificationshardly affect activity

RX = O or S

X = O or S

©Gibot-Leclerc / INRA

(bI) : SL SAR as plant hormone (bII) : S L SAR as AM fungi branching factor

(bIII): SL SAR as root-parasitic seeds stimulant

©Rameau / IN RA

O O

X OO

A BC

D

Stereocheemistryis not important

ABC-rings canbe replaced byan aromatic ring

Substitutions at C3' position in D-ring are tolerated

R

3′

X = O or S

(bI) : SL SA R as plan t hormone

©Le Tacon / INRTT A

O O

O OO

A BC

D


A-ring modificationshardly affect acti vity

R

(bII) : SL SAR a s AM fungi branching factor

O

OR

O

O OO

O O

O

R1

R2

A BC

R1 = Me, R2 = R3 = H, (+)-5-DeoxystrigolR1 = Me, R2 = OH, R3 = H, (+)-StrigolR1 = Me, R2 = O, R3 = H, (+)-StrigoneR1 = Me, R2 = OAc, R3 = H, (+)-Strigyl acetateR1 = CH2OH, R2 = H, R3 = H, (+)-SorgomolR1 = Me, R2 = H, R3 = OH, (+)-Ent -2'-epi-orobancholR1 = Me, R2 = H, R3 = OAc, (+)-Ent -2'-epi-orobanchyl acetateR1 = R2 = R3 = H, (+)-Sorgolactone

910

87

65 4

3a

3

21

8a8b

4a6'

2'

4'

5'

1'

7'

OO

3'D

O

R1

O

O OO

R1 = H, R2 = H, (-)-Ent-2'-epi-5-deoxystrigolR1 = OH, R2 = H, (-)-OrobancholR1 = OAc, R2 = H, (-)-Orobanchyl acetateR1 = OH, R2 = OH, 7-HydroxyorobancholR1 = OH, R2 = O, 7-OxoorobancholR1 = OAc, R2 = OH, 7-Hydroxyorobanchyl acetateR1 = OAc, R2 = O, 7-Oxoorobanchyl acetate

O

OR

O

O OO

R = Ac, (-)-Fabacyl acetateR = H, Fabacol

O

R = H, (-)-SolanacolR = Ac, (-)-Solanacyl acetate

R2

R3

(al) (all)

O OO

Carlactone

(alll)O O

O OO

GR24


Structures of natural SLs and biosynthetic precursor, structure–activity relationship (SAR) data. (aI) Natural SL family with BCD stereochemistry as in

(+)-strigol, the numbers correspond to the numbering of each atom of the SL core, (a–d) correspond to the name of each ring. (aII) Natural SL family

with BCD stereochemistry as in (�)-orobanchol. In (aI), (aII): the pink chemical bonds correspond to the invariable part in the natural SLs. (aIII)

Structure of carlactone and synthetic GR24. SL SAR data (bI) as plant hormone (pea shoot branching), (bII) as AM fungi branching factor, (bIII) as root-

parasitic weed seeds stimulant. In (bI), (bII) and (bIII): R = substitutions on A-ring, * = stereogenic centre. In bold, part of the structure essential for the

bioactivity. The same colours in (bI), (bII) and (bIII) correspond to the same SAR data. Ac = acetyl, Me = methyl.

are very rare, very likely because SL levels are very low in

shoot. Grafting experiments early indicated that SLs

principally produced in roots, but also in the stem, are

transported upward via the xylem to the aerial shoot [26].

This hypothesis is supported by the detection of oroban-

chol in Arabidopsis and tomato xylem sap [27,28]. Inter-

estingly, other SLs, abundant in root extracts, were not

detected in xylem sap suggesting preferential loading in

the xylem possibly involving the ABC transporter, PDR1,

identified in petunia, which may act as a SL exporter



[29�]. Metabolism studies with labelled SLs, identifi-

cation of derived molecules and synthesis for testing their

bioactivity are nevertheless still lacking.

Nonetheless, the recent biochemical and structural studies

suggest a novel mechanism of hormone reception and

signalling among plant hormones (Figure 3) where the

enzymatic activity would be essential to the signalling

pathway [23�]. A similar perception mechanism isdescribed

for karrikins, smoke derived compounds structurally






Figure 3

Lid

do

mai

nC

ore

α/β

hyd

rola

sse

fold

D S

H

D S

H

MAX2

D S

H

D14

SL

A BC

DA B

C

D14 D14 D14

Physiolog ica leffec t

F-BOX RECRU ITMENT

BIND ING GR24 HYDR OLYSE STRUC TUR AL CH ANGE

(formation of an intermed iate)

D DD S

HD

CB

A

5’

A BC

O O

O OO

O

OO

O

OO OH

OH

S97

S97

S97

H

OO

OH

OO

HOD

4’3’

2’

1’

7’

6’

A BC

5′D4′

3′

2′

1′

7′

+

D

OO

O

OO OH

OH

S97

S97H

5′D4′

3′

2′

1′+

+ H2O

PRODUC T 1

PRODUC T 2

D 5′

4′3′

2′

1′

7′

5′

4′3′

2′

1′

7′

D S

HH

DD SS

HH PhD D

DD SS

HHD

C

D

?

(a)

(b)


A model of SL signalling pathway through SL hydrolysis. (a) The proposed SL receptor D14 is an a/b-hydrolase with both binding and enzymatic

activities. Structure of D14 is typical of a/b-hydrolase family with 2 domains: a core a/b-hydrolase fold with 7-stranded b-sheets surrounded by 7 a

helices and a lid of 4 a helices that covers the core domain linked by 2 loops (not shown). The hydrophobic active site pocket contains the conserved

serine (S), aspartate (D), histidine (H) catalytic triad essential for D14 enzymatic and binding activities. Structural change of D14 following SL binding or

hydrolysis would trigger MAX2 F-box protein binding and subsequent degradation via the proteasome of SL-signalling repressors still to be identified.

How MAX2 binds D14 is still not understood. (b) Current proposed model for GR24 hydrolysis by D14 with nucleophilic attack of the D-ring and

formation of an intermediate. The hydroxyl group of the serine residue (S97) of the catalytic triad attacks the SL butenolide ring on position C50 leading

to the transitory opening of the D ring and the release of product 1. A transient intermediate product is generated, covalently linked to the protein by the

serine and rapidly converted in a hydroxyl butenolide (product 2).

related to SL and involved in seed germination [30]. Karri-

kin and SL signalling pathways share the F-box protein

MAX2. However, a D14-like (KAI2) protein, not able to

bind GR24 because of a smaller binding pocket, is proposed

to bind and hydrolyse karrikin [22]. Although the moss

Physcomitrella patens synthesizes and responds to SLs [31�],its genome does not contain a true canonical D14 gene, but

rather several D14-like sequences. D14 and D14-like

sequences probably derived from a common ancestor,

but at present it is not clear at what point during land plant

evolution this duplication occurred [32�]. Other recent

findings question the conservation of biosynthesis and



signalling pathways between vascular and non-vascular

plants.

When did strigolactones appear, and for whatpurpose?Recently, SL production was reported not only in Bryo-

phytes [31�] but also in charales [33�], a group of green

algae (among Charophytes) considered the closest to land

plants (Embryophytes) [34] (Figure 4). Extracts or exu-

dates from other groups of green algae (one group of

chlorophytes and two other groups of charophytes) do not

induce germination of parasitic weeds seeds [33�], which






Figure 4

Mono cots

Eud icots

FlowersSeeds

Roots ?

SL/?

Rhizo

idel

onga

tion

SL/?

Indi

vidua

l

exte

nsio

n

SL/M

AX2;D14

bran

chin

g

Land colonization/AM symbiosis

D14

D14 like

SL

MAX2 (precursor)

Gymnosperms

Ferns

Lycop hytes

BR

YO

PH

YT

ES

Charales

OtherCharoph ytes

300

360

400

450

1200

MYP B

ChlorophytesV

AS

CU

LA

R P

LA

NT

S

EM

BR

YO

PH

YT

ES

s

Hornworts

Liverworts

Mosses

GR

EE

N A

LG

AE

CH

AR

OP

HY

TE

S

**

*

*

*


Proposed scheme for the evolutionary context of SL perception/signalling. Occurrence of both known components (D14 and MAX2) of perception

pathway is indicated. MAX2, present prior Bryophytes divergence, is noted as a precursor as likely not involved in SL perception (our unpublished

results on moss). SL different roles are indicated with dashed lines. SL/? indicates that SL perception proteins are unknown, for rhizoid elongation

(within Charales and Bryophytes) and for control of individual extension (in Moss). Roots? indicates that monophyletic root apparition is still debated.

MYBP: Million Years Before Present.

is so far the most sensitive method to detect SLs. Con-

sequently, SLs were likely to be present before land

colonization.

Besides SLs detection, searches for SL-related genes (or

transcripts) have been performed in green lineage. D27(Figure 1) homologues are present in the genome of all

species from the green lineage, including those that do

not synthesize SLs [33�]. However, in green algae, moss

and Selaginella (Lycophyte) at least, D27 homologues are

non-canonical (D27-like) and may catalyse different reac-

tions or have other functions in these species [35]. In

contrast, genes encoding enzymes catalysing further SL

synthesis steps (Carotenoid Cleavage Dioxygenase genes



CCD7 and CCD8, Figure 1) have only been found in

Embryophytes (including moss), and not in Charales,

for which complete genome sequence is however lacking

[33�]. As the liverwort Marchantia polymorpha lacks the

CCD8 gene, it has been suggested that an alternative

(more ancient) CCD8-independent SL-biosynthesis

pathway would operate in this basal Embryophyte and

in Charales [33�]. It could explain why SLs are still

detected in null ccd8 mutants [31�,36]. Moreover, the

MAX1 gene (Figure 1), encoding a cytochrome P450

[37] is present in all Embryophytes except the moss P.patens and the liverwort M. polymorpha, and absent from

algae genomes ([31�,38], Bowman JL, pers. comm.). As P.patens produces complex decorated SLs (Figure 2 and






[31�]) another P450 may insure MAX1 function, or the last

SL synthesis steps are different in moss, again highlight-

ing flexibility in the SL synthesis pathways [35].

The perception mechanism likely differs between vas-

cular and non-vascular plants. Only D14-like sequences

have been identified in non-vascular plants, and although

MAX2 homologues have been found in all sequenced

Embryophyte genomes, genetic and physiology data

indicate that the moss MAX2 homologue might not be

involved in the SL response in P. patens (our unpublished

results). Genome sequencing and SL quantification data

in other land plants (e.g. hornworts) and algae groups are

needed for a better understanding of the SL pathway

evolution. The recent finding of SLs and related genes in

Charales indicates that these molecules, by favouring

anchorage ability of rhizoids before the apparition of

roots, would have first had a hormonal function on plant

architecture [3,33�].

ConclusionAlthough an understanding of SL signalling has been

rapidly increasing, major questions still remain to be

answered. In particular, the mechanism by which the

probable SL receptor D14 recognizes the MAX2 F-box

protein is not yet known and the putative repressors of SL

signalling have still not been identified. These repressors

are supposed to be targeted for degradation via the 26S

proteasome. Discovering receptors for SL in different

organisms, vascular and non-vascular plants, parasitic

plants and fungi will have significant ecological and

agronomical implications. Particularly, the design of nov-

el SL analogues with specific bioactivity will be of major

interest, for example, analogues with similar bioactivity as

natural SLs for shoot branching and low bioactivity on

parasitic plants [16,17].

AcknowledgementsThe authors thank Rosemary and Jean-Marie Beau for careful reading of themanuscript, Junko Kyozuka for the rice picture and the Agence Nationalede la Recherche (contract ANR-12-BSV6-004-01) for financial support.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

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4.��

Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM,Newcomb RD, Snowden KC: Dad2 is an alpha/beta hydrolase



likely to be involved in the perception of the plant branchinghormone, strigolactone. Curr Biol 2012, 22:2032-2036.

Hamiaux et al. demonstrate that the Petunia a/b hydrolase DAD2, is verylikely the strigolactone receptor with both a binding and an enzymaticactivities. They show that DAD2 interacts with the F-box proteinPhMAX2A, in a strigolactone concentration-dependent manner.

5.��

Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P,Ghisla S, Bouwmeester H, Beyer P, Al-Babili S: The path from b-carotene to carlactone, a strigolactone-like plant hormone.Science 2012, 335:1348-1351.

The authors demonstrate a new biosynthetic pathway for SLs based onthe discovery of carlactone, a SL precursor possessing the A and D rings.They also report that D27 is a b-carotene isomerase.

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9.�

Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S, Akiyama K,Hayashi H, Yokota T, Nomura T, Yoneyama K: Confirmingstereochemical structures of strigolactones produced by riceand tobacco. Mol Plant 2013, 6:153-163.

The authors clearly demonstrate by comparison with natural SLs andsynthetic standards the presence of two chemical families of SLs basedon stereochemistry differences.

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17.�

Boyer FD, de Saint Germain A, Pillot JP, Pouvreau JB, Chen VX,Ramos S, Stevenin A, Simier P, Delavault P, Beau JM, Rameau C:Structure–activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea:molecule design for shoot branching. Plant Physiol 2012,159:1524-1544.

The authors reported here the first SL structure–activity relationshipstudies for inhibition of bud outgrowth based on simple bioassays on pea.

18. Chen VX, Boyer F-D, Rameau C, Pillot J-P, Vors J-P, Beau J-M:New synthesis of A-ring aromatic strigolactone analogues andtheir evaluation as plant hormones in pea (Pisum sativum).Chem Eur J 2013, 19:4849-4857.

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22. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y,Yamaguchi S, Hakoshima T: Structures of d14 and d14l in thestrigolactone and karrikin signaling pathways. Genes Cells2013, 18:147-160.

23.�

Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH, Liu Y, Chen RZ,Kovach A, Kang Y et al.: Crystal structures of twophytohormone signal-transducing alpha/beta hydrolases:karrikin-signaling kai2 and strigolactone-signaling dwarf14.Cell Res 2013, 23:436-439.

The authors obtained the crystal structure of the rice D14 a/b hydrolasebound to a GR24 degradation intermediate.

24. Sun T-p: Gibberellin-gid1-della: a pivotal regulatory module forplant growth and development. Plant Physiol 2010, 154:567-570.

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27. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA,Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C: Strigolactones are transported through the xylem andplay a key role in shoot architectural response to phosphatedeficiency in nonarbuscular mycorrhizal host Arabidopsis.Plant Physiol 2011, 155:974-987.

28. Kohlen W, Charnikhova T, Lammers M, Pollina T, Toth P, Haider I,Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ, Lopez-Raez JA: The tomato carotenoid cleavage dioxygenase8(slccd8) regulates rhizosphere signaling, plant architectureand affects reproductive development through strigolactonebiosynthesis. New Phytol 2012, 196:535-547.

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Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M,Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E:A petunia abc protein controls strigolactone-dependentsymbiotic signalling and branching. Nature 2012, 483:341-344.

The authors show that the Petunia hybrida ABC transporter PDR1behaves as a cellular strigolactone exporter. The Petunia pdr1 mutant



is more branched, is defective in strigolactone exudation but has normalstrigolactone levels in roots.

30. Scaffidi A, Waters MT, Bond CS, Dixon KW, Smith SM,Ghisalberti EL, Flematti GR: Exploring the molecularmechanism of karrikins and strigolactones. Bioorg Med ChemLett 2012, 22:3743-3746.

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Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Nogue F,Rameau C: Strigolactones regulate protonema branching andact as a quorum sensing-like signal in the mossPhyscomitrella patens. Development 2011, 138:1531-1539.

This is the first report of SL occurrence in a non-vascular plant. The resultssuggest a specific role for SL in moss community structure, by regulatingplant size according to individual density. Such function is completelynovel for a plant hormone.

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Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW,Smith SM: Specialisation within the dwarf14 protein familyconfers distinct responses to karrikins and strigolactones inArabidopsis. Development 2012, 139:1285-1295.

Waters et al. demonstrate that the Arabidopsis a/b hydrolase AtD14 isinvolved in strigolactone response whereas the paralogue AtD14-like/KAI2 is required for karrikin response.

33.�

Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C,Lecompte E, Delwiche CF, Yoneyama K, Becard G, Sejalon-Delmas N: Origin of strigolactones in the green lineage. NewPhytol 2012, 195:857-871.

Through a detailed search of SL content/activity and SL-related genesoccurrence in many different species of the green lineage, the authorsshowed that SL were already present in some green algae (Charales) andsuggested that SL primary role was hormonal rather than to promote AMsymbiosis.

34. Bowman JL: Walkabout on the long branches of plantevolution. Curr Opin Plant Biol 2013, 16:70-77.

35. Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O: A role formore axillary growth1 (max1) in evolutionary diversity instrigolactone signaling upstream of max2. Plant Physiol 2013,161:1885-1902.

36. Foo E, Davies NW: Strigolactones promote nodulation in pea.Planta 2011, 234:1073-1081.

37. Booker J, Sieberer T, Wright W, Williamson L, Willett B,Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O: Max1encodes a cytochrome p450 family member that actsdownstream of max3/4 to produce a carotenoid-derivedbranch-inhibiting hormone. Dev Cell 2005, 8:443-449.

38. Nelson D, Werck-Reichhart D: A p450-centric view of plantevolution. Plant J 2011, 66:194-211.













































































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Novel insights into strigolactone distribution and signalling - IJPB - Inra