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Opinion
TRENDS in Plant Science Vol.6 No.9 September 2001
Pectin
methylesterases:
cell wall enzymes
with important roles
in plant physiology
show that PMEs can be analysed at the tissue level
using new methods such as microanalysis on 25-µm
cryosections6,7 or a gel diffusion assay8,9. These
studies have also shown the importance of the acidic
PMEs in plant physiology6,9. Acidic PMEs are barely
detectable among proteins extracted from isolated
cell walls, whereas they are abundant in proteins
eluted directly from tissues10 or from infiltrated
organs11. Because acidic isoforms are probably only
weakly adsorbed onto the cell wall components,
soluble-protein extraction procedures increase their
recovery dramatically6. These observations suggest
that some of the failure to detect acidic isoforms in
higher plants might be related to the experimental
conditions used for protein extraction.
Fabienne Micheli
Pectin methylesterases: a multigene family
Pectin methylesterases catalyse the demethylesterification of cell wall
polygalacturonans. In dicot plants, these ubiquitous cell wall enzymes are
involved in important developmental processes including cellular adhesion
and stem elongation. Here, I highlight recent studies that challenge the
accepted views of the mechanism and function of pectin methylesterases,
including the co-secretion of pectins and pectin methylesterases into the
apoplasm, new action patterns of mature pectin methylesterases and a
possible function of the pro regions of pectin methylesterases as
intramolecular chaperones.
The plant cell wall is an intricate structure involved
in the determination of cell size and shape, growth
and development, intercellular communication, and
interaction with the environment1. The primary cell
wall is largely composed of polysaccharides (cellulose,
hemicelluloses and pectins), enzymes and structural
proteins. Pectins are a highly heterogeneous group of
polymers that includes homogalacturonans and
rhamnogalacturonans I and II (Ref. 2). Pectins form
~35% of the dry weight of dicot cell walls. Pectins are
also abundant in gymnosperm cell walls, but less so
in the walls of grasses3.
It is widely accepted that pectins are polymerized
in the cis Golgi, methylesterified in the medial Golgi
and substituted with side chains in the trans Golgi
cisternae4. Pectins are secreted into the wall as
highly methylesterified forms. Subsequently, they
can then be modified by pectinases such as pectin
methylesterases (PMEs), which catalyse the
demethylesterification of homogalacturonans
releasing acidic pectins and methanol (Fig. 1).
Biochemical study of pectin methylesterases
Fabienne Micheli
Laboratoire de Biologie
Moléculaire des Relations
Plantes–Microorganismes,
INRA–CNRS, BP27,
31326 Castanet-Tolosan
Cedex, France.
e-mail:
[email protected]
Historically, the first PME analyses were made on
PME isoforms purified from plant cell walls using
standard conditions of extraction, assay and
electrophoretic migration from large amounts of
material5. Most of these purified PME isoforms have
neutral or alkaline isoelectric points (pIs), and only a
few studies have revealed the presence of acidic
pectin methylesterases5. However, recent studies
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In the past five years, it has been shown that the
several PME isoforms detected in cell walls are
encoded by a multigene family12,13. Recently, the
systematic sequencing of the Arabidopsis genome
has greatly contributed to the identification of the 67
PME-related genes in this species14. The PME genes
encode pre-pro-proteins that have peptide motifs
considered to be signatures of PMEs. The pre-region
or signal peptide is required for protein targeting to
the endoplasmic reticulum. The pro-PME is secreted
to the apoplasm via the cis, medial and trans Golgi
cisternae, and the trans Golgi network, and only the
mature part of the PME (without the pro region) is
found in the cell wall.
According to recent data from the systematic
sequencing of the Arabidopsis genome14, PME genes
can be divided into two classes. Genes in the first class
contain only two or three introns and a long pro
region, and genes in the other class contain five or six
introns and a short or nonexistent pro region; these
two classes have been called type I and type II,
respectively (L. Richard, pers. commun.). The type II
sequences have a structure close to that of the PMEs
identified in phytopathogenic organisms (bacteria,
fungi) and are involved in cell wall soaking during
plant infection. Such data force us to consider the role
and development of the PME pro region.
An intramolecular chaperone?
Because it has been observed that cell-wall-extracted
PMEs do not have a pro region15 (Fig. 2c), cleavage of
the pro region from the mature PME might occur
either early on, before excretion of the mature PME
into the apoplasm (Fig. 2a), or later (Fig. 2b). In the
first case, the pro region might be degraded (Fig. 2d)
or play a role either inside the cell (Fig. 2e) or in the
apoplasm (Fig. 2f ). Although the role of the pro region
is not known, several hypotheses are possible. It
might play a role: (1) in the biological function of
PMEs; (2) in targeting PMEs towards the cell wall;
(3) as an intramolecular chaperone, allowing
conformational folding of the mature part of the PME
(Ref. 16); or (4) as an inhibitor of the enzyme activity
1360-1385/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(01)02045-3
Opinion
Fig. 1.
Demethylesterification of
pectins by pectin
methylesterases (PME).
TRENDS in Plant Science Vol.6 No.9 September 2001
COOCH3
O
O
415
COOH
OH
O
COOCH3
O
OH
OH
2 H2O
2 CH3OH
O
O
OH
O
PME
OH
COOH
O
O
OH
OH
O
OH
TRENDS in Plant Science
carried out by the mature PME. However, at present
there is no evidence that the pro region is correlated
with the suggested roles (2) and (4).
Although experimental evidence to support the
view that the pro regions of PMEs are intramolecular
chaperones is lacking, the arguments in Table 1 could
be applied to PMEs, supporting the hypothetical role
of the PME pro region in inhibiting the mature part of
the protein and protein folding. Moreover, it can be
hypothesized that the pro region could inhibit the
mature part during its secretion to the apoplasm to
prevent premature demethylesterification of pectins
before their insertion in the cell wall (Fig. 3). This
point is particularly interesting because the isoforms
involved in microsporogenesis and pollen tube growth
are type II PMEs related to bacterial PMEs (Refs 17,18).
Comparison of PME action patterns between pollen,
Pro-PME
cis
Medial
Golgi
trans
(d)
(a)
(a)
(e)
(b)
?
(f)
Cytoplasm
(c)
?
Cell wall
TRENDS in Plant Science
Fig. 2. Hypotheses for pectin methylesterase (PME) excretion into the apoplasm and maturation of
the protein. The cleavage of the pro region (red) from the mature PME (green) occurred either early
on, before excretion of the mature PME into the apoplasm (a,c), or afterwards (b). In the first case,
the pro region could be degraded (d) or play a role either inside the cell (e) or in the apoplasm (f).
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during pollen tube growth, and phytopathogenic
bacteria, during plant infection, show that both PMEs
were involved in plant cell wall soaking19. This action
pattern during ‘invasion’ could characterize PMEs
that do not have a pro region. Indeed, this hypothesis
agrees with the fact that the inhibition of PME
activity was not necessary during protein excretion
by bacteria, because they did not secrete pectins.
Mode of action of mature pectin methylesterases
After their integration into the cell wall, mature
PMEs could have different modes of action. For
20 years, the commonly accepted hypothesis
concerning the mode of action of PMEs on
homogalacturonans was that they could act either
randomly (as in fungi) or linearly (as in plants)
along the chain of pectins20. When PMEs act
randomly on homogalacturonans, the
demethylesterification releases protons that
promote the action of endopolygalacturonases21
and contribute to cell wall loosening. When PMEs
act linearly on homogalacturonans, PMEs give rise
to blocks of free carboxyl groups that could interact
with Ca2+, so creating a pectate gel4. Because the
action of endopolygalacturonases in such a gel is
limited, this action pattern of PMEs contributes to
cell wall stiffening.
Because acidic PMEs were thought to be
essentially confined to fungi, the simplest hypothesis
was that random demethylesterification depended on
acidic PMEs, whereas linear demethylesterification
depended on alkaline PMEs. However, more recent
studies have shown that PME activity also depends
on pH and the initial degree of methylesterification of
the pectins. Some isoforms can act randomly at acidic
pH but linearly at alkaline pH. And, at a given pH,
some isoforms are more effective than others on
highly methylesterified pectins22,23. Moreover, PME
activity is enhanced by cations: trivalent cations are
more effective than bivalent cations, which are
themselves more effective than monovalent cations24.
Depending on their concentration, cations might also
modify the affinity of PMEs for their substrate.
In conclusion, the action pattern of mature PMEs is
regulated in the cell wall by numerous factors that both
reveal the complexity of the enzymes and challenge the
simplistic hypothesis that divides the PMEs into two
groups: ‘alkaline, linear demethylesterification’ and
‘acidic, random demethylesterification’ (Fig. 4).
Opinion
416
TRENDS in Plant Science Vol.6 No.9 September 2001
Table 1. Comparison of the characteristics of intramolecular chaperones and pectin methylesterasesa
Function
Intramolecular chaperone
Pectin methylesterases (PMEs)b
Essential requirement for protein
folding
Yes
?
Catalytic activity (in vivo reusability)
No
It has not been shown that PME activity is provided from the pro
region. All active microsequenced PMEs were mature proteins49,50.
ATP requirement
No
?
Interaction with the folded protein
Competitive inhibitor
The pro region could inhibit the mature part during its secretion to the
apoplasm to prevent premature pectin demethylesterification before
their insertion in the cell wall.
Specificity for mediating folding
Highly specific
Pro regions of PMEs do not have high homologies and are variable in
size and sequence according to the isoform, suggesting specificity of
the pro region with respect to the corresponding mature part.
Folding mechanism
Numerous mechanisms depending
on the protein and the conditions
in which the folding is made
?
Released via a proteolytic cleavage
Comparison between polypeptidic sequences of cell wall extracted
PMEs, and the open-reading-frame of the corresponding gene shows
that the proteolytic cleavage of the pro region is made close to the
RR(K)LL motif conserved in every plant PME (Ref. 50). This motif is
highly conserved with the cleavage site (RRKRR) found in some
intramolecular chaperones from animals51.
Association with the protein to be folded Covalently attached to the N-terminus The mature part of PMEs is covalently attached to the pro region.
aData
from Ref. 16.
marks indicate data not known.
bQuestions
Regulation of pectin methylesterase activity
Pectins
Pro-PME
In addition to the possible role of the pro region as
an inhibitor of PME activity during the secretory
pathway, and to the regulation of the pectin
demethylesterification in the cell wall, it has been
shown that there are inhibitors of PME activity in
the cell wall25,26. PME activity is also regulated by
hormones. Auxin-induced PME activity increases cell
wall extension and, as a result, water absorption by
the cell27,28. Some contradictory results have been
obtained about the role of abscisic acid (ABA) on PME
regulation. For example, although ABA enhanced
PME activity in tomato seeds8, it inhibited PME
activity during seed germination in yellow cedar
(Chamaecyparis nootkatensis)9. Moreover, in these
cedar seeds, gibberellic acid (GA3) had a stimulatory
effect on PME activity9.
cis
Medial
Golgi
trans
?
?
Structure of pectin methylesterases
Cytoplasm
Cell wall
Regulation (e.g. pH, ions)
TRENDS in Plant Science
Fig. 3. Hypothesis of co-secretion of the pectins and the pectin methylesterases (PME) into the
apoplasm. In this scheme, the pro region (red) could inhibit the mature part (green) during its
secretion to the apoplasm to prevent premature demethylesterification of pectins before their
insertion into the cell wall. Methylesterified galacturonic acids are represented in blue and
demethylesterified galacturonic acids in yellow.
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A better understanding of the pectin–PME interaction
could be obtained by overexpression followed by analysis
of the structure of PMEs using X-ray crystallography.
Thus, PMEs from phytopathogenic bacteria and fungi
have been produced in heterologous prokaryotic29 and
eukaryotic30 systems. The lack of data showing higher
plant PME overexpression shows that, during export
towards the apoplasm, plant PME isoenzymes probably
undergo organism-specific post-translational processing
that is necessary for their structural and functional
integrity. As a consequence, the functional
characterization of the PME-related genes identified to
date is generally difficult and requires alternative
methods based on the overexpression of the genes in
heterologous plant systems31.
Opinion
Fig. 4. Modes of action
of pectin methylesterases
(PMEs). Depending on
the cell wall properties,
the mature PMEs (green)
can act randomly (a),
promoting the action of
pH-dependent cell wall
hydrolases such as
endopolygalacturonases
(PG) and contributing to
cell wall loosening, or can
act linearly (b), giving rise
to blocks of free carboxyl
groups that interact with
bivalent ions (Ca2+), so
ridigifying the cell wall.
Methylesterified
galacturonic acids are
represented in blue and
demethylesterified
galacturonic acids in
yellow.
TRENDS in Plant Science Vol.6 No.9 September 2001
417
Cytoplasm
Cell wall
?
(a)
Ca2+
Regulation by
pH, ions, pectin
methylesterification degree
PG
(–)
(+)
(b)
Ca2+
PG
(+)
(–)
Ca2+ Ca2+ Ca2+ Ca2+
Ca2+ Ca2+ Ca2+ Ca2+ Ca2+ Ca2+
Cell wall loosening
Cell wall rigidification
TRENDS in Plant Science
In view of the difficulty of overexpressing a plant
PME gene in a heterologous system, the structure of
a plant PME protein has been predicted by in silico
methods32. This model, established by comparison with
the three-dimensional structure of a crystallized pectin
lyase from Aspergillus niger33, revealed that the PME
is a β-helix protein that is characterized by secondary
elements of parallel β sheets coiled into a large righthanded cylinder (Fig. 5). This model is closest to the
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structures observed for other pectinases that have
already been analysed crystallographically34–36 and
has recently been confirmed by the preparation of
crystals of bacterial PME (Ref. 37).
Ubiquitous enzymes involved in many physiological
processes
Several studies have shown a strong correlation
between PME activity or PME gene expression and
418
Fig. 5. Homology model
of the three-dimensional
structure of a plant pectin
methylesterase. This is a
β-helix protein
characterized by
secondary elements of
parallel β sheets (yellow)
coiled into a large righthanded cylinder and by a
loop with α helix (red).
Also shown are four
highly conserved
tryptophan residues
(TRP, light-green) and four
strictly conserved tyrosine
residues (TYR, white),
which are probably
involved in binding the
substrate. Three
conserved phenylalanine
residues (PHE, pink) are
shown within the
molecule, which are
important in forming the
hydrophobic core of the
parallel β helix32.
Acknowledgements
I thank Nigel Chaffey
(University of Bristol, UK)
for critical reading of the
manuscript. I am grateful
to Renée Goldberg, Luc
Richard and Marianne
Bordenave (Université
Pierre et Marie Curie,
France) for helpful
discussions during the
past four years. Research
support was provided by
the commission of the
European Communities,
Agriculture and Fisheries
(FAIR) specific RTD
programme (CT 98-3972).
It does not necessarily
reflect the Commission’s
views and in no way
anticipates the
Commission’s future
policy in this area.
Opinion
TRENDS in Plant Science Vol.6 No.9 September 2001
Pectin methylesterases in cellular adhesion
During separation of the border cells of the root cap of
pea, PME activity increases and is correlated with an
increase in the amount of acidic pectin and a decrease
in cell wall pH (Ref. 45). This study was performed
using an antisense transgenic plant transformed
with a PME gene (rcpme1) obtained by screening a
root cDNA library46. Analysis of transgenic plants
showed that rcpme1 expression is required for the
maintenance of extracellular pH, elongation of the
cells within the root tip and for cell wall degradation
leading to border cell separation.
Pectin methylesterases in stem elongation
physiological processes such as fruit maturation38,
microsporogenesis and tube pollen growth39,40,
cambial cell differentiation6,41, seed germination9
and hypocotyl elongation15. Interestingly, two recent
studies have shown unequivocally that a PME is a
host-cell receptor for the tobacco mosaic virus (TMV)
movement protein42,43. Thus, the interaction between
the virus movement protein and the PME is
required for viral cell-to-cell movement through
plasmodesmata. One hypothesis proposed is that
binding of the TMV movement protein interferes
with PME activity, altering the cell wall ion balance
and consequently inducing changes in the
permeability of the plasmodesmata43. Furthermore,
studies using mutants permit a more specific
characterization of the physiological involvement of
PMEs in plant development, as illustrated below.
Pectin methylesterases as a methanol source
In 1998, a close correlation was reported between
PME activity and levels of methanol in fruit tissues
from both wild-type tomato and a PME antisense
mutant, indicating that PME is on the primary
biosynthetic pathway for methanol production in
tomato fruit44. Because methanol oxidation to CO2
could result in the incorporation of methanol carbon
into metabolites via the Calvin–Benson cycle, PMEs
could play an appreciable, albeit indirect, role in the
photosynthetic metabolism of the plant.
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