www.landesbioscience.com Plant Signaling & Behavior 636
Plant Signaling & Behavior 7:6, 636-641; June 2012; © 2012 Landes Bioscience
MINI-REVIEW
Introduction
Flavonoids are secondary metabolites derived from the phenyl-
propanoid pathway and >9,000 flavonoids have been character-
ized in plants.
1
Major subgroups of flavonoids that are found
in most higher plants include chalcones, flavones, flavonols,
anthocyanins, proanthocyanidins (condensed tannins) and
aurones.
2,3
Diverse functions of flavonoids include UV protec-
tion, sexual reproduction process, defense and flower coloring.
Even if complex, the biosynthesis of these molecules has been
well described and numerous enzymatic steps are involved (Fig.
1).
4,5
In Arabidopsis most enzymes implicated in flavonoid bio-
synthesis are encoded by single copy genes, whereas in most plant
species most genes occur in multigene families.
6
Flavonoids are
synthesized in the cytosol,
7
stored in vacuoles,
8
and they are also
known to be present in external rhizosphere through exudation.
9
Moreover, flavonoid synthesis is organ and tissue-dependent, and
is affected by environmental conditions, such as light intensity,
temperature and nitrogen.
10-12
Flavonoids accumulate specifi-
cally in dividing cells in the root, for example in the lateral root
*Correspondence to: Valérie Hocher; Email: valerie.hocher@ird.fr
Submitted: 03/13/12; Accepted: 03/15/12
http://dx.doi.org/10.4161/psb.20039
Flavonoids are a group of secondary metabolites derived from
the phenylpropanoid pathway. They are ubiquitous in the
plant kingdom and have many diverse functions including key
roles at diferent levels of root endosymbioses. While there
is a lot of information on the role of particular lavonoids in
the Rhizobium-legume symbiosis, yet their exact role during
the establishment of arbuscular mycorrhiza and actinorhizal
symbioses still remains unclear. Within the context of the
latest data suggesting a common symbiotic signaling pathway
for both plant-fungal and plant bacterial endosymbioses
between legumes and actinorhiza-forming fagales, this
mini-review highlights some of the recent studies on the
three major types of root endosymbioses. Implication of the
molecular knowledge of endosymbioses signaling and genetic
manipulation of lavonoid biosynthetic pathway on the
development of strategies for the transfer and optimization of
nodulation are also discussed.
The role of lavonoids in the establishment of
plant roots endosymbioses with arbuscular
mycorrhiza fungi, rhizobia and Frankia bacteria
Khalid Abdel-Lateif, Didier Bogusz and Valérie Hocher*
Equipe Rhizogenèse; UMR DIADE (IRD, UM2); Institut de Recherche pour le Développement (IRD); Montpellier, France
Key words: flavonoids, endosymbiosis, legume-rhizobium symbioses, actinorhizal symbioses, arbuscular mycorrhiza, signaling
and nodule primordia of subterranean clover ( Trifolium subter-
raneum),
13,14
in the root tip and the lateral root primordia of
Arabidopsis.
15,16
Plant roots form three major types of intracellular endosymbi-
oses in symbiotic relationships with arbuscular mycorrhizal (AM)
fungi of the group of Glomeromycecota and with nitrogen fixing
bacteria of the genus Rhizobium and Frankia. At least 80% of all
angiosperms are able to participate in AM symbiosis while only
ten families of angiosperms are known to form symbiotic asso-
ciation with nitrogen-fixing bacteria in root nodules.
17
In addi-
tion to occurring with rhizobia in the legumes and Ulmaceae,
nitrogen-fixing symbioses involving root nodules also occur
with Frankia in some members of Betulaceae, Casuarinaceae,
Coriariaceae, Datiscaceae, Elaeagnaceae, Myricaceae, Rhamnaceae
and Rosaceae. Molecular phylogeny of plant groups that engage in
root nodule symbiosis shows that they all belong to a single clade,
the Fabid (Eurosid 1).
18
Some features of root nodule endosym-
biosis could have been recruited from the more ancient AM sym-
biosis.
19,20
Hence, the question of shared mechanisms including
the control of early signaling events is raised.
21,22
Orchestration
of these early events requires the exchange of signaling mol-
ecules. The rhizobial signal molecule, the so-called nodulation
(Nod) factors are lipochitooligosaccharides (LCOs), consisting
of an N-acetylglucosamine backbone, N-acylated on the termi-
nal non-reducing sugar and bearing different substitutions on
the oligosaccharidic backbone that is symbiosis specific.
23
In the
case of actinorhizal symbiosis, Frankia signals are unknown.
24,25
However, it has been previously shown that Frankia alni
(ACN14a) produces a root hair deforming factor (RHDF) in
culture supernatant that reacts with Alnus glutinosa root hair
cells inducing branching and curling of root hair cells.
26
This
factor was shown to have a molecular weight below 3,000 da, to
be heat-stable (similar to Rhizobium Nod factor) but also to be
hydrophilic and to resist to chitinases (contrary to Rhizobium
Nod factor). In AM symbiosis, it has been suggested that LCOs
produced by the AM fungus could have a role in the establish-
ment of AM symbiosis.
27
The work on the diversity and the role
in discriminating specificity of LCOs produced by AM fungus is
still in progress.
27
The recent availability of genomic resources in
AM fungi is opening new possibilities to characterize the genes
involved in the synthesis of signaling molecules.
28