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320
Role of lectins (and rhizobial exopolysaccharides) in
legume nodulation
Ann M Hirsch
The lectin recognition hypothesis proposes that plant lectins
mediate specificity in the Rhizobium–legume symbiosis.
Although the hypothesis was developed eight years before nod
genes were identified in rhizobia and sixteen years before Nod
factor was shown to be a major determinant of host specificity,
experiments performed recently using transgenic lectin plants
support its main tenets.
Addresses
Department of Molecular, Cell and Developmental Biology, and
Molecular Biology Institute, University of California, Los Angeles, CA
90095-1606, USA; e-mail: [email protected]
such as adenine and derivatives, the cytokinins, which function as plant growth regulators [6,7].
Lectins correlate with the cross-inoculation groups established by their source legume [8]. Rhizobia that nodulate
Phaseolus vulgaris were found to interact with bean lectin
[1], whereas soybean lectin bound and aggregated 22 of
25 strains of Bradyrhizobium (previously known as
Rhizobium) japonicum that nodulate soybean [2]. Twentythree other bradyrhizobial strains that were not
aggregated by SBL (soybean lectin) did not initiate nodule formation on soybean.
Current Opinion in Plant Biology 1999, 2:320–326
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© Elsevier Science Ltd ISSN 1369-5266
Abbreviations
Ccd
cortical cell divisions
CPS
capsular polysaccharides
EPS
exopolysaccharides
Had
root hair deformation
LPS
lipopolysaccharides
PRA
peanut root lectin
PSL
Pisum sativum lectin
SBL
soybean lectin
Introduction
The lectin-recognition hypothesis, championed by
Hamblin and Kent [1], Bohlool and Schmidt [2], and
Dazzo and Hubbell [3], was formulated to explain host
specificity between legume and rhizobial symbiotic partners. It was based on the strong correlation between the
inoculation specificity of bacteria of the family
Rhizobiaceae on their legume hosts and the ability of hostproduced lectins to bind to Rhizobium cells, and soon
became accepted as ‘dogma’. The concept and the diagrammatic scheme shown in Figure 1 were incorporated
into numerous textbooks, and although there were exceptions to the idea that plant lectins mediated specificity, the
hypothesis has held for more than 20 years.
In this review, I will give a brief overview of the lectin
recognition hypothesis, the experiments that confirm it,
and offer some suggestions as to future research directions.
The lectin recognition hypothesis was formulated many
years before the isolation and characterization of nod genes
in rhizobia as well as before Nod factor was recognized as
mediating legume-Rhizobium specificity. Generic Nod factor is an N-acetyl-glucosamine oligomer (with a backbone
of three to five glucosamine units) and an acyl tail of differing lengths and saturation, depending on the rhizobial
species. Various other substituents can be present on the
reducing end [9] (see WJ Broughton and X Perret, this
issue pp 305–311). Specificity resides in both the reducing
and non-reducing ends of the molecule. On alfalfa, Nod
factor alone, at a very low concentration (10–12 M), elicits
root hair deformation (Had), whereas a higher concentration (10–7 M) is required for extensive cortical cell divisions
(Ccd) [10]. Although many legumes undergo the Had
Figure 1
Root hair wall
R. trifolii
Clover
lectin
Root hair
cytoplasm
Cross-reactive antigen
Why lectins?
Lectins were originally defined as carbohydrate-binding proteins of non-immune origin that agglutinate cells and/or
precipitate glycoconjugates [4]. This definition has been
modified for plant lectins to include those proteins possessing at least one noncatalytic domain that binds reversibly to
a specific mono- or oligosaccharide [5]. Most plant lectins are
multivalent. Some also bind small hydrophobic molecules
Current Opinion in Plant Biology
The lectin cross-bridge model of Dazzo and Hubbell [3], showing how
clover lectin links the cross-reactive antigens of the rhizobia with those
of the plant.
Role of lectins in legume nodulation Hirsch
response in response to Nod factor, only a few (alfalfa,
Glycine soja, Phaseolus, Acacia, Lotus corniculatus) undergo
Ccd [10–12,13••].
One of the advantages of studying lectins is that the characteristics of these proteins, as well as the oligosaccharides
that bind to them, are well known. On the basis of its
structure, Nod factor is thus an unlikely ligand for a typical legume lectin like SBL or Pisum sativum lectin PSL. In
contrast, a novel 46 kDa root lectin isolated from Dolichos
bifloros is shown to bind to Nod factors produced by rhizobia that nodulate this legume [14•]. It has no similarity
in sequence to any other lectins yet described. Moreover,
it functions as an apyrase catalysing the hydrolysis of
phosphoanhdride bonds of nucleoside di- and triphosphates [14•]. A Nod factor-binding site, enriched in
plasma membrane fractions isolated from Medicago cell
suspension cultures has also been reported (see Note
added in proof). However, as yet, no correlation has been
made with the loss of function of a particular binding protein and a non-nodulation locus, so it is not clear yet
whether or not these binding proteins/sites are essential
for the symbiotic interaction.
Lectins are found in the right place and at the
right time
Most plant lectins are secreted proteins and are found in
vacuoles, cell walls, or intercellular spaces. Although they
are found in just about every plant organ, their distribution
in root tissue gives the most support to the lectin recognition hypothesis — lectins are localized to root hairs, which
are the sites of rhizobial entry for many legumes [15–20].
They are most frequently found at the tips of developing
root hairs, although Díaz et al. [18] localized PSL to root
hair precursor cells.
Root and seed lectins can be the product of a single gene.
This is the case for soybean (Glycine max) [21] and its
lectin SBL (or SBA) and pea (Pisum sativum) and its lectin
PSL (or PSA) [22]. DNA gel blot hybridization and S1
nuclease analysis and ribonuclease protection experiments (used for fine-structure mapping and accurately
determining the steady-state level of any mRNA) failed
to identify any functional lectin genes in soybean other
than Le1, the gene encoding SBL [21]. Although several
papers suggested that there is a separate soybean root
lectin, we were unable to find one. Our attempts to isolate a root protein that was reported to cross-react to an
antibody made to SBL failed. Although we used the same
antibody as Vodkin and Raikhel [23], the protein that we
isolated had a high degree of sequence similarity to the
acidic ribosomal protein P0 [24]. Thus, if there is a root
lectin in soybean, it must be quite different from the protein encoded by Le1. The presence of another lectin may
also explain why ‘Sooty’, a soybean cultivar with a mutant
lectin gene (le1) nodulates [25], and why root exudate
from Sooty reverses the delayed nodulation phenotype of
B. japonicum strain HS111 in the same way as the lectin
321
derived from Le1 soybeans [26]. Another lectin composed
of 45 kDa subunits with specificity for 4-O-methylglucuronic acid [27,28] has been detected in soybean, but
the gene encoding it remains unidentified. However,
‘Sooty’ has been tested only with high concentrations of
inoculum (S Pueppke, personal communication). Will it
nodulate with a below-threshold number of bradyrhizobia
or with bradyrhizobia that do not attach properly (see
later section)?
What bacterial component binds to
legume lectins?
Rhizobia are typical Gram-negative bacteria with a cytoplasmic and outer membrane enclosing a periplasmic space.
Much of their outer surface is composed of polysaccharides:
lipopolysaccharides (LPS), capsular polysaccharides (CPS
or KPS), and acidic exopolysaccharides (EPS). Mutants that
are defective in the production of these polysaccharides are
often blocked in inducing nodule development, particularly in steps involving nodule invasion via infection threads.
A considerable amount of data show that rhizobial surface
polysaccharides bind to some lectins.
Although not specifically identifying the factor that
binds to lectin, Bhuvaneswari and Bauer [29] found that
culture conditions for B. japonicum influenced the
expression of surface receptors for SBL and that these
potential lectin receptors were transiently expressed.
Dazzo and Truchet [30] found similar results. The transiently expressed lectin receptors were found to be
acidic and neutral polysaccharides or lipopolysaccharides, depending on the rhizobia.
An alfalfa lectin isolated from seed extract by Kamberger
[31] was found in agarose gel diffusion tests to interact with
Rhizobium (Sinorhizobium) meliloti LPS, but not with LPS
from heterologous rhizobia. Jayaraman and Das [32]
reported that the peanut root lectin (PRA II) bound to LPS
of peanut-specific bradyrhizobia, and not to other
Bradyrhizobium species.
New life for the lectin recognition hypothesis
The experiments of Díaz et al. [33] revitalized interest in
the lectin recognition hypothesis. Transgenic white
clover roots carrying the pea lectin gene were nodulated
by the heterologous strain R. leguminosarum bv. viciae,
whereas no nodules formed on clover plants that lacked
the pea gene. Altering the carbohydrate-binding domain
of the introduced lectin by site-directed mutagenesis
demonstrated that lectin mediated this heterologous
interaction. When transgenic plants carrying the mutated,
transgenic lectin were inoculated with the heterologous
rhizobia, no nodules formed [34].
We [13••] expanded the applicability of these experiments
by investigating soybean and Lotus corniculatus [35], two
legumes that are distantly related. We transferred Le1 into
L. corniculatus, which is normally nodulated by
322
Biotic interactions
of the bradyrhizobial cell surface must bind to SBL.
Although B. japonicum USDA110 induced nodules on the
roots of the transgenic Lotus, neither B. elkanii USDA31,
which does not bind SBL, nor B. japonicum exoB mutants,
attached to the Lotus roots or induced nodules over the levels demonstrated by the control plants [13••]. These results
suggested that mediation of host specificity occurs via
lectin interacting with an exopolysaccharide component of
the rhizobial cell surface.
Figure 2
(a)
(b)
Aggregation
(c)
Attachment
(d)
Shepherd's crook
formation
Infection thread
development
Current Opinion in Plant Biology
Diagram of how lectin is presumed to function in the transgenic plants
carrying a foreign lectin gene. After Kijne [51]. (a) Lectins (Y) are
localized to and secreted from the emerging root hair facilitating
rhizobial aggregation. (b) The rhizobia are attached to the root hair.
(c) The root hair curls around the rhizobia and an infection thread
forms at the ‘hyaline spot’. The rhizobia are bound by lectin within the
nascent thread. (d) The infection thread extends and the root hair
elongates. Rhizobia multiply within the thread.
Mesorhizobium loti. Experiments on the transgenic L. corniculatus showed the following: first, SBL was expressed
in the emerging root hairs in the susceptible zone of the
root; second, when the transgenic Lotus roots were inoculated with B. japonicum, nodules formed, probably
because of the high concentration of heterologous Nod
factor brought about by the accumulation of bradyrhizobia
at the root hair tips. However, the nodules were devoid of
bacteria because infection threads aborted; third, if the
sugar-binding site of Le1 was mutated and transgenic
plants carrying the mutated lectin gene were inoculated
with B. japonicum, no nodules developed even though the
defective lectin was properly targeted to the root hair tip.
The bradyrhizobia did not attach to these root hairs [13••],
and, presumably, a high concentration of heterologous
Nod factor was no longer present at the root hair tip.
These experiments indicated that lectins mediate one level
of host specificity, and furthermore, that some component
If exopolysaccharide is a ligand for lectin, one would predict that Exo– rhizobia would be unable to attach to plant
root hairs or to elicit infection thread formation. The former is not true, most likely because other rhizobial
proteins also function in adhesion (see references in
[36]). However, the latter is frequently true. Inoculation
with rhizobial exopolysaccharide mutants phenocopies
the nodules developed by the transgenic lectin plants.
Uninfected nodules develop in response to Exo–
mutants because infection threads abort [37,38••]. For
Sinorhizobium meliloti strain 1021, succinoglycan appears
to be essential for colonization of the root hair. Mutants
that either do not produce or overproduce succinoglycan
fail to form proper infection threads [38••]. Exo– mutants
of R. leguminosarum bv. trifolii also elicit uninfected
nodules [39,40•].
How is lectin mediating specificity in the transgenic
plants? One possibility is that lectins are a ‘glue’ that
attaches the rhizobia to a site on a susceptible root hair,
in this way providing a point source of rhizobial-produced signal molecules. First, secreted lectin aggregates
the rhizobia and facilitates their attachment to the root
hair (Figure 2). Next, the bacteria elicit infection thread
formation even though they produce a heterologous Nod
factor. Nod– rhizobia do not induce infection threads or
induce Ccd on the transgenic roots, arguing for the
involvement of Nod factor in these processes [13••].
That infection threads are formed in the root hairs of the
transgenic plants suggests that lectins mediate rhizobial
attachment even within the thread (Figure 2).
Nevertheless, even though the lectin and the surface
polysaccharides are complementary, the threads abort
and the nodules are uninfected, suggesting that there is
some required response that is not duplicated in the
transgenic plants. One possibility is that the transgenic
lectin may not be properly integrated into a nodulation
signal transduction pathway.
Plant receptors for lectins?
Lectins bind glycoconjugates found on the surfaces of foreign organisms. Indeed, lectins may serve as a sort of
‘cloaking’ device thereby facilitating the entry of a pathogenic microorganism. Brelles-Marino et al. [41] found that
infection thread development was enhanced when R. etli
was incubated with bean seed lectin. Does lectin mask rhizobial cell surface components such that the root hair cell
takes up these foreign cells?
Role of lectins in legume nodulation Hirsch
Figure 3
(a) Uninoculated root hair:
lectin and Nod Factor
receptors.
(c) Rhizobia added to root
hair: the hair curls
(e) Uninoculated root hair:
lectin associates with a
transmembrane receptor
(b) Purified NF added to root
hairs: the hair deforms.
(d) Enlargement of (c). Both
lectin and NF receptors
bind to rhizobial cell.
(f) Enlargement of (c). Binding of
lectin to rhizobal cell causes
lateral migration of receptors.
Current Opinion in Plant Biology
Two possible models to explain the involvement of lectin in infection
thread formation. In the first model, (a–d), lectin acts as a ‘glue’.
(a) Lectins (Y) and putative Nod factor receptors (ξ) are randomly
distributed on the uninoculated root hair tip. (b) If Nod factor (NF)
alone is added, the root hairs deform because Nod factor binds to its
receptor, but the receptors do not migrate laterally within the plasma
membrane. (c) In the presence of rhizobia, root hairs curl.
(d) Enlargement of boxed area in (c). Lectin molecules bind to rhizobial
surface molecules concentrating the source of Nod factor. Nod factor
receptors cap after binding to Nod factor due to its localized
production. Capping activates the signal transduction pathway. In the
second model (e,f), lectins directly interact with another component.
(e) Lectins bound to transmembrane proteins are randomly distributed
on the uninoculated root hair top. (f) When the lectin binds the
rhizobial surface polysaccharides, the attached proteins cap. This
event is Nod factor-dependent because infection threads do not form
in its absence.
323
A larger question is how the bacteria are engulfed once
they make contact with the root hair. The lectins used to
formulate the lectin recognition hypothesis have no transmembrane domains that could connect directly to
components of a signal transduction cascade. Legume seed
lectins are usually hololectins with two or more carbohydrate-binding sites, one per subunit; the carbohydrate
binding domains are identical or very similar [42]. Proteins
that bind to legume lectins (potential lectin receptors)
have been detected in seeds (see references in [8]), but
minimal information exists on their subcellular location
[43]. The significance of these protein associations is also
largely unknown.
It is possible that lectins function in signal transduction
pathways by binding to transmembrane proteins. Metcalf
et al. [44] found that soybean protoplasts bound several
iodinated lectins specifically and saturably. Fluorescence
microscopy of the protoplasts showed uniform labeling of
the plasma membrane implying that the lectins bound to
transmembrane receptors. The lectin–receptor complexes
were mobile, as demonstrated by photobleaching studies,
and mild trypsinization of the soybean protoplasts
removed SBL, but not other lectins [44]. These findings
demonstrate that receptors specific for SBL are localized to
the plasma membrane.
A gene encoding a new class of receptor-like kinase has
been cloned from Arabidopsis [45]. It appears to be a
member of a superfamily of genes that define a new class
of plant serine/threonine receptor kinases (see Note
added in proof). What makes this putative receptor
kinase unusual is that, on the basis of sequence information, the extracellular domain is homologous to a legume
lectin, and has binding sites for sugars and for small
hydrophobic molecules ([45]; see Note added in proof).
However, there are also some significant differences
from legume lectins based on molecular modelling, such
as the lack of a Ca2+ binding site, which may be coupled
to a lack of monosaccharide binding activity (see Note
added in proof).
Are there proteins in legumes similar to the Arabidopsis
lectin–kinase, or do legume lectins exist as soluble proteins that interact with transmembrane kinases once a
ligand is bound? Ridge et al. [46••] tested the binding of
several lectins with affinities for different sugars on root
hairs of uninoculated legumes. They found that five of ten
tested lectins bound to the broad-host range legume siratro (Macroptilium), whereas only one lectin bound to each
of the narrow-host range plants, except for white clover,
which bound two. No lectins bound to Arabidopsis root
hairs. Sugars at the tips of the root hairs probably exist as
glycoconjugates that are transiently expressed. What are
these sugar-binding molecules at the root hair tip and are
they involved in rhizobial entry? Could they be part of the
signal transduction chain?
324
Biotic interactions
Conclusions and predictions
As it stands, the lectin recognition hypothesis — with a
few modifications — has withstood the test of time. The
question remains, however, as to whether lectin is merely a glue that holds the rhizobia and the plant in close
contact until Nod factor works its wonders, or whether it
plays an active role in specificity by transmitting a signal
to one or both symbiotic partners. For example, Kijne
and co-workers [47] proposed that lectins may be
involved in stabilizing the cell cytoskeleton by transmembrane interactions. When lectin binds rhizobia, the
root hair tip becomes destabilized and an infection
thread can form.
Figure 3 illustrates other possibilities. In an uninoculated
root hair (Figure 3a), Nod factor receptors and lectins are
randomly distributed in and along the membrane of the
root hair tip. Adding Nod factor by itself does not cause
receptors/binding proteins to migrate even though Nod
factor is bound to them; thus, the root hair deforms but
does not curl (Figure 3b). When rhizobia are added, the
root hair curls around the attached bacteria (Figure 3c).
Attachment facilitated by lectins binding to their polysaccharide coats concentrates the rhizobia at a spot on the root
hair. Nod factor synthesized by the rhizobia then binds to
specific receptor/binding proteins that migrate laterally
and form a focused cap (Figure 3d). The size of the cap
dictates the strength of the ensuing signal transduction
pathway and whether or not the rhizobia will be taken up
into the infection thread [48].
In another model, lectins complex with transmembrane
proteins, which, in the uninoculated root, are distributed
randomly at the root-hair tip (Figure 3e). Upon inoculation, the lectin binds to the rhizobial surface and then
interacts via a protein-binding domain with the putative
transmembrane protein. The complexes cap and, in the
process, the transmembrane proteins transmit the signal
through an as yet uncharacterized nodulation signal transduction pathway (Figure 3f). Nod factor is still required for
rhizobial entry because even though nodules develop,
bona fide infection threads do not form without rhizobia
contacting the root hair cell membrane. However, the
effect of Nod factor may be independent of a receptor or
binding protein. It is known that Nod factor can modify
the biological activity of the root hair cell even in the
absence of rhizobia (see references in [9]). Whether or not
it does this through an external Nod Factor receptor/binding protein as indicated in Figure 3b or via another
mechanism is unknown.
One test of the above possibilities is to determine whether
cv. ‘Sooty’ nodulates in response to a low concentration of
wild-type bradyrhizobia or to exoB B. japonicum. If there is
too little Nod factor brought about by the reduced binding
of bradyrhizobia to Sooty root hairs, then the roots will not
form nodules.
Many of the components needed for rhizobial endocytosis
have been found in legume root hair tips. In addition to
lectin, numerous features that are involved in mediating
bacterial invasion into host cells — actin, microtubules,
clathrin, and various vesicles — have been detected [49,50].
However, we are still missing the critical components of the
signal transduction pathway, although attempts to find
them are underway. Then, it may be possible to test
whether lectins play an active role in propagating a signal
that leads to nodule development.
Note added in proof
Two papers have recently been published that are highly
relevant to this review [52•,53•]. See main text for details.
Acknowledgements
My thanks to Stefan J Kirchanski, Thomas A LaRue, and Robert W
Ridge for reading the manuscript and for their constructive comments. I
also want to thank Jan Kijne for insights and the members of my
laboratory for their helpful comments. Special thanks go out to those lab
members, past and present, who have worked or are working on the
lectin project. I am especially grateful to Margaret Kowalczyk for
preparing the figures. My apologies to authors whose work I have not
cited due to space constraints. Research in the author’s laboratory on
lectins is funded by the National Research Initiative Competitive Grant
Program, Grants No. 93-37305-9144 and No. 96-35405-353 from the
Nitrogen Fixation/Metabolism program.
References and recommended reading
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• of special interest
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Biotic interactions
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requirements of Nod factor for binding. Although recognition is mediated by
both the lipid and oligosaccharide components of the Nod factor molecule,
surprisingly, NFBS2 is not selective for the reducing end-sulfate group, which
normally is essential for Medicago root hair deformation and nodulation.
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Characterization of the Arabidopsis lecRK-a genes: members of
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domain homologous to legume lectins. Plant Mol Biol 1999,
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This paper is a follow-up on the previous observation [45] made by this
group that Arabidopsis has a receptor-like kinase (RLK) with an extracellular domain homologous to legume lectins. The previous paper [45] was
the first report of a kinase with a lectin domain. The RLKs are glucosylated and localized to the plasma membrane fraction, but their function(s) is
(are) unknown.