75
REVIEW
BIOLOGICALLY-ACTIVE CELL WALL MATERIALS
1
2
EUNICE MELOTTO and JOHN M. LABAVITCH
Pomology Department, University of California, Davis, CA, 95616, USA.
ABSTRACT- Cell wall-derived oligosaccharides have been
identified as active inducers of a variety of physiological
responses in many different plant tissues. At first, they were
shown to be involved in phytoalexin accumulation, an important
process by which plants protect themselves against attack of
microorganisms. Subsequently, a number of other
mechanisms of plant resistance to pathogens were reported
as being regulated by wall fragments, including synthesis of
inhibitors of insect proteinases, and deposition of extracellular
molecular barriers to invading organisms such as lignin and
hydroxyproline-rich glycoproteins. The discovery that
oligosaccharides can influence plant growth and differentiation
has brought new insight into the initial work of plant pathologists
on carbohydrates with biological functions, conjunctively
denoted as oligosaccharins. Relatively recent results have
yielded some information which suggests that fruits can ripen
in response to oligosaccharides derived from the digestion of
their own cell wall. Wall fragments have been shown to hasten
not only the climacteric peak of ethylene of ripening tissues but
also other ripening-associated changes such as appearance
of red color and climacteric CO2.
Additional index terms: Oligosaccharins, plant defense, growth,
differentiation, ripening, second messengers.
MATERIAIS DA PAREDE CELULAR COM
ATIVIDADE BIOLÓGICA
RESUMO- Oligossacarídeos originados da parede celular têm
sido identificados como sendo indutores de diversas respostas
fisiológicas em muitos tecidos vegetais. Primeiramente, foi
demonstrado que estavam envolvidos no acúmulo de
fitoalexinas, um processo importante pelo qual plantas se
protegem contra o ataque de microrganismos.
Subsequentemente, vários outros mecanismos de defesa
contra patógenos mediados por fragmentos da parede celular
foram descritos. Esses incluem síntese de inibidores de
proteinases de insetos, e deposição de barreiras
extracelulares como lignina e glicoproteinas ricas em
hidroxiprolina. A descoberta de que oligossacarídeos podiam
influenciar crescimento e diferenciação em plantas
proporcionou novo rumo ao trabalho inicial de fitopatologistas
em carboidratos com funções biológicas, coletivamente
denominados oligossacarinas. Resultados relativamente
1Received on 18/01/1994 and accepted on 03/02/1994.
2Departamento de Botânica, ESALQ-USP, CP 09, Piracicaba, SP,
13418-900, Brazil.
recentes têm originado informações que sugerem o controle
do amadurecimento de frutos por oligossacarídeos derivados
de suas próprias paredes celulares. Fragmentos da parede
aceleram não somente o aparecimento do pico climatérico de
produção de etileno como também outras mudanças
associadas ao amadurecimento, como o desenvolvimento da
cor vermelha em certos frutos e o pico climatérico de CO2.
Termos adicionais para indexação: Oligossacarinas, defesa
de plantas, crescimento, diferenciação, amadurecimento,
mensageiros secundários.
INTRODUCTION
For many years, the cell wall was considered a rigid,
static portion of the plant cell whose only function was
to provide physical support and protection for the
plasma membrane and cell contents.
However,
relatively recent areas of research have provided novel
evidence for the dynamics of the cell wall structure,
although its complexity is still beyond our
understanding. Particularly striking are the studies
which led to the conclusion that fragments of plant cell
wall polymers have regulatory effects within plant
tissues. The several biological functions that can be
controlled by such molecules described thus far include
host defense responses to pathogens, cell growth, and
morphogenesis ( reviewed in Darvill & Albersheim,
1984; McNeil et al., 1984; Aldington et al., 1991; Ryan
& Farmer, 1991). More recently, it has been suggested
that fruit ripening could also be controlled by the action
of cell wall-derived materials (Campbell & Labavitch,
1989; Melotto et al., 1992, 1993, 1994).
THE ROLE OF CELL WALL-DERIVED
MATERIALS ON PLANT DEFENSE
MECHANISMS
The specific and potent biological effects of cell wall
derived oligosaccharides on living plant cells was first
demonstrated in the 1970’s by plant pathologists.
Studies on interaction between pathogenic fungi and
their host plants indicated that oligosaccharides derived
from fungal cell wall could elicit the synthesis of
antimicrobial compounds, so-called phytoalexins, by the
plant cells (Ayers et al., 1976a,b; Ebel et al., 1976;
Sharp et al., 1984). It has further been shown that low
molecular weight fragments derived from the walls of
R. Bras. Fisiol. Veg., 6(1):75-82, 1994.
76
higher
plants
are
active
as
well.
Pectic
polysaccharide-degrading enzymes secreted by either
fungi or bacteria were able to trigger plant defense
responses by releasing active pectic fragments from the
plant cell wall. West and colleagues (Lee & West,
1981a,b; Bruce & West, 1982) have shown that an
endopolygalacturonase (endo-PG) isolated from the
fungus Rhizopus stolonifer was able to release a pectic
fragment from seedlings of castor beans (Ricinus
communis L.), which in turn elicited the synthesis of an
antifungal agent, casbene. At approximately the same
time, Albersheim and co-workers (Davis et al., 1982,
1984) demonstrated that a bacterial pathogen, Erwinia
carotovora, produced a pectic-degrading enzyme,
endopolygalacturonic acid (PGA) lyase, which elicited
phytoalexin production in soybeans. It was concluded
that an oligogalacturonide released from the plant cell
wall by the bacterial enzyme was a required
intermediate in the process of phytoalexin elicitation.
Additional experiments have shown that partial acid
hydrolysis of soybean cell walls as well as citrus pectin
yields fragments composed of galacturonosyl residues
which are also active in inducing phytoalexin production
(Nothnagel et al., 1983).
Cell wall-derived fragments are now known to be
potentially involved in a number of other processes by
which plants protect themselves from pathogenic
microbes and insects. Pectin fragments have been
shown to induce the synthesis of inhibitors of insect
proteinases, which may protect the plant by decreasing
the insect’s ability to digest leaf protein (Bishop et al.,
1981, 1984; Walker-Simmons & Ryan, 1986; Ryan,
1992).
Oligosaccharides have also been reported to play a
role in plant resistance to pathogens by activating the
deposition of extracellular molecular barriers to invading
organisms. There are reports of elicitation of lignin
biosynthesis in cucumber hypocotyls (Robertsen, 1986;
Robertsen & Svalheim, 1990) and suspension cultures
of castor bean cells (Bruce & West, 1989) after their
treatment with pectic fragments, which mimics, in part,
infection by an invasive organism. It has been shown
that endo-PG from the scab fungus Cladosporium
cucumerinum is able to elicit lignification in cucumber
hypocotyls,
presumably
by
releasing
an
oligogalacturonide elicitor from the plant cell wall
(Robertsen, 1987). In fact, secretion of pectin-degrading
enzymes is a widespread, important factor for pathogen
penetration into plant tissues (Darvill & Albersheim,
1984). Therefore, treatment of plant cells with pectic
fragments would most likely simulate one aspect of
microbial digestion of plant cell wall pectin during
infection.
The deposition of hydroxyproline-rich glycoproteins
(HRGP’s), an important structural component of plant
cell walls, also increases in response to infection. The
accumulation of HRGP’s has been reported to be
triggered by both fungal and plant cell wall elicitors
(Roby et al., 1985; Showalter et al., 1985). In melon
(Cucumis melo L. cv Cantaloupe), ethylene seems to
mediate this response since it increases early in
elicitor-treated plant material, and an inhibitor of its
synthesis, aminoethoxyvinylglycine (AVG), prevents the
elicitation of HRGP’s (Roby et al., 1985). Ethylene
production in response to elicitor treatment has been
observed in other systems as well. VanderMolen et al.
(1983) have shown that castor bean explants
synthesized ethylene when treated with wall-degrading
enzymes, produced by a vascular wilt pathogenic
fungus, Fusarium oxysporum. The plant’s defense
mechanism observed in response to the enzymes
and/or infection, plugging of the xylem vessels, did not
occur if ethylene synthesis was inhibited. More recently,
ethylene has been documented to be induced in
ripening fruits by wall-derived elicitors, in the absence of
pathogens. This will be discussed in greater detail in a
later section of this review.
Another well known defense mechanism triggered by
oligosaccharides is the hypersensitive necrosis
response, i.e., a rapid induction of cell death in the
vicinity of the infection site. Phytotoxic plant cell wall
fragments have been detected in maize (Brucheli et al.,
1990) and cowpea pods (Cervone et al., 1987) when
inoculated with pectin-degrading enzymes from the rice
blast fungus (Magnaporthe grisea) and from Aspergillus
niger, respectively. It has been hypothesized that
invading parasites enzymically solubilize fragments
from the plant cell wall, which the plant can recognize as
danger signals. As a consequence, a small number of
cells at the site of attack quickly die, which results in the
arrest of further growth of the pathogen (McNeil et al.,
1984).
THE ROLE OF CELL WALL-DERIVED
MATERIALS ON GROWTH AND
DIFFERENTIATION
One of the most exciting discoveries that followed the
initial work of plant pathologists on naturally occurring
carbohydrates with biological functions, conjunctively
denoted as oligosaccharins, was their possible role on
the control of growth and differentiation. In their studies,
York and colleagues (1984) provided interesting data
which suggested the involvement of xyloglucan
oligosaccharides in the plant development. An endo-β
1,4-glucanase-digested xyloglucan isolated from
suspension-cultured sycamore (Acer pseudoplatanus)
cells inhibited auxin-stimulated elongation of etiolated
pea stem segments. The active component was a
nonasaccharide which contained glucose, xylose,
galactose, fucose and arabinose in the ratio of
4.0:3.0:1.4:1.0:0.1. It was then speculated that the
release of xyloglucan fragments during auxin-promoted
cell wall loosening (Labavitch & Ray, 1974) would act in
a feedback control loop, preventing excessive growth.
This idea was strengthened by subsequent findings in
another laboratory. Fry (1986) demonstrated the in vivo
formation of a xyloglucan nonasaccharide (XG9) in
R. Bras. Fisiol. Veg., 6(1):75-82, 1994.
77
cell-suspension cultures of spinach which was identical
to the xyloglucan-derived nonasaccharide associated
with anti-auxin activity (York et al., 1984). Two years
later, McDougall & Fry (1988) confirmed the high
specificity of the XG9 in inhibiting the auxin-promoted
growth of etiolated pea segments. Since an
heptasaccharide (XG7) did not interfere with the
inhibitor action of XG9, and it was known to be present
in vivo (Fry, 1986), the authors suggested that the auxin
antagonism was controlled at the level of a highly
discriminating receptor. Additional experiments have
shown that octa- and deca-saccharides (XG8 and
XG10) neither have anti-auxin activity nor interfere with
the XG9 action (1989). For a comprehensive review on
structure-activity relationships of xyloglucan fragments
as well as a number of other biologically active
oligosaccharides refer to Aldington et al. (1991).
Surprising results have recently provided evidence for
a second role of XG9. McDougall & Fry (1990) have
demonstrated that XG9 can mimic auxin activity by
activating an enzyme, cellulase, thereby promoting cell
growth during elongation. Such an effect was also
exhibited by other oligosaccharides produced by fungal
digestion of xyloglucans. The optimal concentration of
XG9 for the growth-promoting effect was 1 µM whereas
the concentration for the anti-auxin effect was only 1 nM.
This peculiar dose-response curve suggests a rather
complex mechanism for xyloglucan regulation of auxin
activity.
Fry and co-workers (1992) have later reported the
occurrence of a novel enzyme activity in several plant
extracts, xyloglucan endotransglycosylase - XET, which
may play an important role on the mechanism of plant
growth. This enzyme is able to catalyze the transfer of
a high MW portion from a xyloglucan to a
xyloglucan-derived oligosaccharide such as XG9. In
view of these findings, the authors have suggested that
xyloglucan oligosaccharides enhance growth due to
their ability to keep the wall ’loose’ during the action of
XET rather than their ability to activate cellulase, as
initially thought (McDougall & Fry, 1990).
Oligomers derived from fungal endo-PG digestion of
pectin have also been shown to interfere with the
auxin-induced elongation of pea stems (Branca et al.,
1988). In this case, the concentration required for
inhibition was much greater than that for XG9. The
authors have suggested that the ability of pectin
oligomers to interfere with the auxin action might be
relevant when defense mechanisms are triggered in
higher plants. In support of their hypothesis, there are
observations of an increase in auxin levels in several
host-parasite systems. Moreover, as discussed earlier in
this review, there is significant secretion of fungal
pectin-degrading enzymes which digest the plant cell
wall, potentially releasing oligomers that are capable of
triggering a variety of defense responses. Additionally,
those oligomers could interact with auxin produced upon
infection.
A very recent report which corroborates the work by
McDougall & Fry (1988, 1989), has indicated that XG9
exhibits in vivo anti-auxin activity in a system other than
the pea stem segments. XG9 derived from cell walls of
suspension-cultured cells of carrots (Daucus carota L.)
affected the regeneration of carrot protoplasts
(Emmerling & Seitz, 1990), when applied to the medium
in nanomolar concentrations. The effects were similar to
those achieved by auxin depletion of the regeneration
medium. Either the absence of auxin or the addition of
XG9 in a medium containing auxin resulted in reduced
viability of the protoplasts. The authors have suggested
that protoplasts would provide an excellent system for
elucidating the mechanisms of action of XG9.
The effects of oligosaccharins in plant development
have also been shown by the ability of pectic fragments
to control both the morphological characteristics of
tobacco thin-layer (TLC) cultured cells (Tran Thanh Van
et al., 1985; Eberhard et al., 1989) and flowering of
Lemna gibba (McNeil et al.,1984). The exposure to
fragments caused the TLC’s to form vegetative shoots
rather than flowers or callus, and flowers rather than
vegetative shoots, depending upon the composition of
the medium (Tran Than Van et al., 1985). At different
auxin and kinetin concentrations, pectic fragments
either inhibited root formation or induced tissue
enlargement and the formation of flowers (Eberhard et
al., 1989). The effects of pectic fragments could not be
explained by their interference with the availability of
auxin or cytokinin to the TLC’s. Their mechanism of
action remains undefined, as are those of others well
known plant hormones.
In the case of Lemna gibba (duckweed), it has been
shown that pectic fragments from suspension-cultured
sycamore cells are able to inhibit the development of
flowers and promote vegetative growth (McNeil et al.,
1984).
Cell Wall Oligosaccharides as Elicitors
of Ripening
In the past few years, there has been some work
showing that low molecular weight wall fragments are
capable of promoting ethylene production of fruits
(Brecht & Huber, 1988; Tong & Gross, 1988, 1990;
Campbell & Labavitch, 1991a; Melotto, 1992, Melotto et
al., 1992, 1993, 1994), and fruit cells (Tong et al., 1986;
Campbell & Labavitch, 1991b). The substantial amount
of research on the catabolic metabolism of the cell wall
has already clearly shown that wall hydrolases may play
an important role on affecting wall structure and tissue
firmness during fruit ripening. The additional information
that cell wall breakdown products can trigger ethylene
biogenesis, an authentic regulator of the ripening
process (Tucker & Grierson, 1987), suggests that cell
wall hydrolases may have functions beyond that of
determining textural changes in the fruit.
Tong et al. (1986) have reported one of the earliest
studies of the effect of hydrolases and their products on
R. Bras. Fisiol. Veg., 6(1):75-82, 1994.
78
ethylene production of fruit cells. From their results, it
was suggested that oligouronides solubilized during
ripening of fruits may play a role in the climacteric rise
of ethylene. The system used in their studies was
suspension-cultured pear cells, which have been
documented to exhibit senescence or “ripening”
phenomena in vitro, by manipulation of the culture
medium (Pech & Romani, 1979; Romani, 1987).
Nevertheless, it was pointed out that there are
limitations for the use of suspension cultures as an
assay system. The same hypothesis was tested in
whole tomato fruits by Brecht and Huber (1988) and
Baldwin and Pressey (1988). Preclimacteric fruits were
vacuum-infiltrated with either pectic fragments
enzymically released from ripe tomato fruit cell wall
(Brecht & Huber, 1988) or tomato pectin-lysing enzymes
(Baldwin & Pressey, 1988). Infiltration of pectin
fragments into the fruits not only hastened the
climacteric peak of ethylene but also accelerated other
ripening-associated changes such as appearance of red
color, and climacteric carbon dioxide. Oligouronides
excluded from Bio-Gel P-2 (degree of polymerization DP - higher than 8) exhibited greater ripening-promotive
activity, compared to the mixtures with a DP from 1 to 3,
and from 4 to 6. The studies with pectin-lysing enzymes
have shown that both PG1 and PG2 induced ethylene
production in green “cherry” tomato fruit as well as in the
mutants rin, nor, and Cornell 111 (Baldwin & Pressey,
1988). The effects of PG2 was more pronounced than
that exhibited by PG1. Pectinmethylesterase (PME)
alone did not elicit ethylene synthesis but it was
observed to enhance PG2’s effect when added to PG
treatments. Although there is evidence for an increase
in ethylene synthesis prior to the appearance of PG
(Brady et al., 1982; Grierson & Tucker, 1983; Su et al.,
1984), it was suggested that trace amounts of PG,
undetectable by the currently used methodology, might
be present in green fruit. Very low quantities of PG
would be sufficient to raise ethylene levels to a certain
internal threshold, which in its turn, would promote
increased synthesis of PG and ethylene (autocatalysis).
The reciprocal promotion of PG and ethylene synthesis
would account for the extremely high levels of these two
compounds observed during the climacteric. Embodied
in this hypothesis is the observation that ethylene
induces PG biosynthesis (Grierson & Tucker, 1983) as
well as its own synthesis.
exocarp cells, whereas ripening of exocarp tissues may
be the result of ethylene biosynthesis.
The first attempt to purify and characterize an
endogenous trigger of ethylene production and ripening
has been made by Tong & Gross (1990).
Vacuum-infiltration
of
carbonate-soluble,
covalently-bound pectin (CBP) into both normal and rin
mutant whole, mature green tomato fruit induced an
increase in ethylene production. Rin tomatoes
developed an attenuated red pigmentation in addition to
increased ethylene production. Fractionation of CBP,
extracted from mature green fruit, by DEAE-Sephadex
and Bio-Gel P-100 chromatography led to the recovery
of a partially purified active material which contained
mostly non-cellulosic neutral sugars (95%), and low
contents of uronic acid (less than 5%) and amino acids
(less than 1%). The moiety responsible for the activity
was not identified. Two possibilities were proposed to
explain the mechanism of action of the elicitor. The least
probable was the degradation of the elicitor and
consequent release of free galactose, which would
stimulate ethylene production. Galactose itself has been
reported to induce ethylene biosynthesis (Gross, 1985;
Kim et al., 1987). However, the amounts of galactose
required for elicitation were too high to account for the
polymeric elicitor’s activity. The second hypothesis was
that the elicitor would promote de novo synthesis of PG,
which
would
release
oligouronides
with
ethylene-inducing activity. This hypothesis was more
attractive since, as mentioned before, this class of
molecules has already been shown to stimulate
ethylene production in fruit tissues.
The putative regulatory function of pectin oligomers on
the ripening phenomenon was further addressed in the
work by Melotto (1992) and Melotto et al. (1992, 1993,
1994). These authors have found that active pectin
oligomers naturally occur at the onset of ripening of
tomato fruit. Ethylene-inducing pectic oligomers were
isolated from tomato fruits by both low speed
centrifugation of pericarp discs and homogenization of
pericarp sections, at three progressive stages of
maturity (mature green, breaker, and red). Active
oligomers varied in their amount and composition of
neutral sugar substitutions. It was suggested that the
structural requirements for the biological activity were
not stringent since a range of molecular sizes was
capable of promoting ethylene, the most effective being
oligouronides of DP > 8. A subsequent study on their
probable metabolic origin has revealed that active
oligomers can be generated in vitro by PG treatment of
tomato pectins (Melotto et al., 1993). CDTA-soluble
pectin from cell wall of mature green tomato was not
digested by the enzyme, whereas PG treatment of the
Na2CO3-soluble fraction produced active oligomeric
material of the same size classes as those extracted
from the fruit (Melotto et al., 1992). It is presently known
that the Na2CO3-soluble pectic materials are the pectin
class which changes the most during ripening of tomato
fruit (Carrington et al., 1993). This suggests that the
Campbell and Labavitch have also shown that pectic
oligomers elicit ethylene biosynthesis in both
suspension- cultured pear cells (1989, 1991b), and
tomato pericarp discs (1989, 1991a). In their work with
tomato, acid-hydrolysis generated pectic oligomers (DP
= 5-13 and 6-19) induced an advance in ripening
processes as indicated by an increased reddening and
a long-term, persistent increase in climacteric ethylene
of mature green fruit pericarp discs. Endocarp tissues
responded differently to oligouronides as compared to
exocarp tissues. This observation led to the suggestion
that ripening of the endocarp region may be directly
regulated by pectic oligomers released from adjoining
R. Bras. Fisiol. Veg., 6(1):75-82, 1994.
79
Na2CO3-soluble fraction is the main pectic component
accessible to PG in vivo. Therefore, it is possible that
active oligouronides are generated by PG digestion of
this particular group of pectins at the time of ripening.
Their probable role in the ripening process is yet to be
demonstrated.
THE SEARCH FOR ACTION
MECHANISMS OF OLIGOSACCHARINS
It has been suggested that oligosaccharins can act as
long-distance hormones. This idea evolved from the fact
that pectic oligosaccharides released in an injured leaf
could induce a defense response in neighboring
uninjured leaves (Bishop et al., 1981). However, studies
with radiolabeled fragments (degrees of polymerization
as low as 6) have shown that pectic substances are not
exported from a treated leaf (Baydoun & Fry, 1985).
Therefore, it was concluded that either poly- or
oligosaccharides cannot be long-distance hormones
themselves. An obvious suggestion that followed was
that low molecular weight wall fragments are primary
signaling molecules which induce the release , or
synthesis and release, of a second (long-distance)
messenger. Thus far, the best known candidate for a
second messenger in the transduction of extracellular
signals in plants is the calcium messenger system.
Calcium is known to regulate many enzymic and
physiological processes either directly or in concert with
a calcium-binding protein such as calmodulin (Marme,
1982). It is now generally accepted that changes in
cytosolic free calcium, in response to external stimuli,
can be perceived by the cells which translate them into
physiological responses (Poovaiah et al., 1987).
Furthermore, calcium has been recognized to
participate in the regulation of important transduction
mechanisms in plants such as protein phosphorylation
and accelerated turnover of inositol phospholipids
(Poovaiah et al., 1987; Morse et al., 1989). In view of
these facts, there has been an increasing attempt to
associate the calcium messenger system with the
mechanism of action of oligosaccharins.
A number of investigations has recently dealt with the
possible role of plasma membrane protein kinases in the
signaling
of
plant
defensive
genes
by
oligogalacturonides (Farmer et al., 1989, 1990, 1991).
Both fungal and plant oligosaccharides have been
shown to activate a large spectrum of genes encoding
proteins which are involved in plant defense responses
(Lawton & Lamb, 1987; Ryan, 1988; Ryan & An, 1988).
There are indications that protein phosphorylation may
be a mechanism of signal processing leading to gene
activation. Dietritch and co-workers (1990) have shown
that cytoplasmic, microsomal and nuclear proteins
undergo rapid and transient phosphorylation following
treatment of suspension-cultured parsley (Petroselinum
crispum) cells with fungal elicitor. The changes in protein
phosphorylation, observed as early as 1 minute after
treatment, were dependent on the presence of calcium
in the medium. Fragments of polygalacturonic acid were
also able to trigger the phosphorylation of a plasma
membrane-associated protein from tomato and potato
(Farmer et al., 1991). Active fragments were of the same
length as the uronides that are able to elicit a variety of
defensive and developmental responses in plants.
Based on the ability of such fragments to complex with
calcium in solution, it was suggested that
uronide-calcium complexes interact with the plasma
membrane to signal transduction events leading to the
expression of specific genes.
The primary interaction of an elicitor with a plasma
membrane-located target site has already been
demonstrated in soybean tissues (Schmidt & Ebel,
1987; Cosio et al., 1990; Cheong & Hahn, 1991). A
glucan elicitor derived from a fungal pathogen of
soybean, Phytophthora megasperma, exhibited a
high-affinity, saturable and reversible binding to
membrane fractions of soybean roots (Schmidt & Ebel,
1987). A specific binding site for an heptaglucoside was
also identified in soybean microsomal membranes
(Cheong & Hahn, 1991). The binding was competitively
inhibited by elicitor-active oligoglucosides ranging in
size from hexa- to deca-glucoside.
The identification of a putative receptor for an
oligosaccharin provides evidence for a role of the
plasma membrane as the site of the initiation of signal
transduction events. However, its mode of coupling to
intracellular processes remains to be determined.
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