Molecular Plant Advance Access originally published online on August 20, 2009
Molecular Plant 2009 2(5):851-860; doi:10.1093/mp/ssp066
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Homogalacturonan Methyl-Esterification and Plant Development
a Heidelberg Institute for Plant Science, Im Neuenheimer Feld 360, 69120 Heidelberg, Germany
b Laboratoire de Biologie Cellulaire, Institut Jean-Pierre Bourgin, INRA Centre de Versailles-Grignon, Route de St Cyr, 78026 Versailles, France
c EA3900-BioPI Biologie des Plantes et contrôle des Insectes ravageurs, Université de Picardie, 33 Rue St Leu, 80039 Amiens, France
1 To whom correspondence should be addressed. E-mail gregory.mouille{at}versailles.inra.fr, fax 33 1 30 83 30 99.
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Abstract |
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Abstract
THE HOMOGALACTURONAN, ITS...The ability of a plant cell to expand is largely defined by the physical constraints imposed by its cell wall. Accordingly, cell wall properties have to be regulated during development. The pectic polysaccharide homogalacturonan is a major component of the plant primary walls. Biosynthesis and in muro modification of homogalacturonan have recently emerged as key determinants of plant development, controlling cell adhesion, organ development, and phyllotactic patterning. This review will focus on recent findings regarding impact of homogalacturonan content and methyl-esterification status of this polymer on plant life. De-methyl-esterification of homogalacturonan occurs through the action of the ubiquitous enzyme ‘pectin methyl-esterase’. We here describe various strategies developed by the plant to finely tune the methyl-esterification status of homogalacturonan along key events of the plant lifecycle.
Key Words: Carbohydrate metabolism • cell walls • Arabidopsis • Pectin
Received for publication May 27, 2009. Accepted for publication July 13, 2009.
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THE HOMOGALACTURONAN, ITS BIOSYNTHESIS AND ROLE IN PLANT DEVELOPMENT |
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Structure of Homogalacturonan
The plant cell wall is a highly sophisticated structure formed by a complex mixture of polysaccharides, proteins, and other polymers assembled into a rigid, yet dynamically organized, network. The primary cell wall is composed of cellulose microfibrils embedded in a highly hydrated polysaccharide matrix, which is derived from two major classes of polysaccharides, hemicelluloses, and pectins. Pectins of higher plants form the structurally most complex family of polysaccharides in nature. They make up 35% of the primary cell wall in dicotyledonous plants and non-graminaceous (non-grass) monocots, 2–10% of grass primary walls, and up to 5% of wood tissues (Mohnen, 2008). Pectin has been shown to be involved in plant growth, morphogenesis, organogenesis, development, cell–cell adhesion, defence, leaf abscission, fruit maturation and dehiscence, seed hydration, and ion binding (Ridley et al., 2001; Willats et al., 2001). Five classes of pectinaceous polysaccharides can be distinguished: homogalacturonan (HG), xylogalacturonan (XGA), apiogalacturonan (AP), and rhamnogalacturonan I and II. Rhamnogalacturonan I is the only pectin not built on a HG backbone, but rather on a polymer of galacturonic acid (GalA) and rhamnose (Rha) disaccharide subunits. Homogalacturonan is the most abundant pectic polysaccharide, constituting 65% of total pectin. It consists of a linear
-1,4-linked GalA homopolymer with a typical degree of polymerization of 
100. Despite an apparently very simple linear structure, much remains to be discovered on the specific features and roles of HG. First, HG was considered for many decades as backbone of pectin, linked to RGI. But it was also suggested that HG could form side chains of RGI (Vincken et al., 2003). However, this model was questioned recently after the publication of the work of Coenen et al. (2007). Resolving this controversy constitutes a critical point, since HG as backbone or as side chains will not contribute in the same way to the 3-D structure of the pectin matrix and will consequently affect cell wall structure and properties differently. Another critical feature of HG that influences its properties is the acetylation and methyl-esterification of specific carbons (C2-C3 and C6, respectively) that occur on GalA during synthesis of the backbone.
Biosynthesis of Homogalacturonan
Not much is currently known about the biosynthesis of HG or pectins. The HG is assumed to be synthesized in the cis-Golgi, methyl-esterified in the medial-Golgi, substituted in the trans-Golgi, and secreted in a highly methyl-esterified state (Zhang and Staehelin, 1992; Staehelin and Moore, 1995; Sterling et al., 2001). S-adenosyl methionine and UDP–GalA transporters are supposed to import the necessary precursors into the Golgi. HG GAlactUronosylTransferase (GAUT) and a Pectin Methyl-Transferase (PMT), probably acting as hetero complex, could be involved in the polymerization of a fully methyl-esterified HG (i.e. 80%), which is supposed to be the secreted form. Recently, a Golgi-localized HG GAlactUronosylTransferase has indeed been identified in Arabidopsis (Sterling et al., 2006). Although a Golgi pectin methyl-transferase activity has been shown (Goubet et al., 1998; Ishikawa et al., 2000) and a candidate gene has been identified (Mouille et al., 2007), PMT activity of heterologously expressed protein remains to be demonstrated. Altogether, the current knowledge of the sub-cellular location of the enzymes responsible for HG polysaccharide biosynthesis is scarce.
Homogalacturonan and Plant Development
What is, however, well demonstrated is the key role of HG in maintaining a correct cell adhesion in vivo. Two mutants, quasimodo1 and quasimodo2, carrying mutations in a GAUT (GAUT8) and in a putative Pectin Methyl-Transferase, respectively, were shown to be affected in cellular adhesion (Bouton et al., 2002; Mouille et al., 2007). In quasimodo2 the cell adhesion defect was related to a 25% decrease in the absolute amount of HG in the cell wall without modification of the methyl-esterification rate of the HG. Although the biophysical determinants explaining the impact of HG content on cell adhesion are poorly understood, it was shown that a decrease in HG content leads to an increased flexibility of pectins (Ralet et al., 2008). This property cannot be related to the mechanical properties of the cell wall or the cell adhesion defect of the quasimodo mutants. Such a strong phenotype suggests that the HG content of the cell wall must be timely and temporally regulated during plant development.
After secretion, HG is not distributed uniformly across the cell wall (Willats et al., 2001; Bosch et al., 2005; Parre and Geitmann, 2005b) and HG microdomains of different methyl-esters patterns can be visualized in distinct regions of the cell wall by specific antibodies (Willats et al., 2001). In particular, a stretch of a minimum of nine un-methyl-esterified galacturonic acid residues can form Ca2+ linkages, which may promote the formation of the so-called ‘egg-box’ model structure (Liners et al., 1989). The presence of these ‘egg-box’ structure are assumed to induce gel formation and thus strengthen the wall, or become a target for pectin-degrading enzymes such as polygalacturonases (PG, EC 3.2.1.15
[EC]
) and pectin/pectate lyases (PL, EC 4.2.2.10
[EC]
; EC 4.2.2.2
[EC]
), which act by hydrolyzing the -1,4 link between GalA. Hence, the methyl-esterification status of HG can have dramatic consequences on cell wall texture and mechanical properties, thereby regulating cellular growth and cell shape. Interestingly, pectin methylesterification is subject to significant change during development. This is especially evident in fruit in which the degree of methylesterification decreases during ripening (Barnavon et al., 2001; Brummell and Harpster, 2001; Wakabayashi et al., 2003; Draye and Van Cutsem, 2008). Apparently, the abundance of homogalacturonan with a low level of esterification is also increased in order to compensate for a lack of cellulose, both after treatment with cellulose synthesis inhibitors (Manfield et al., 2004) and in response to reduced cellulose synthase expression (Burton et al., 2000).
Pectic oligogalacturonides (OGAs), small breakdown products of homogalacturonan, have been shown to act as signaling molecules, both as elicitors during pathogen attack (Hahn et al., 1981; Nothnagel et al., 1983; Ridley et al., 2001) and as a hormone-like compound counteracting the effects of auxin during plant development (Branca et al., 1988; Bellincampi et al., 1996; Ridley et al., 2001). It is widely assumed that short, active OGs (Moloshok et al., 1992) are produced by pectate lyase and polygalacturonase-mediated breakdown of HG (Cote et al., 1998) and this breakdown is dependent on distinct patterns of de-methyl-esterification (Wakabayashi et al., 2000, 2003). Recently, it has been shown in strawberry that activity of OGs requires de-methyl-esterification by a pectin methyl-esterase (Osorio et al., 2008).
Thus, the tight control of the methyl-esterification status of HG appears not only to be a key component regulating its biophysical properties, but also to induce the formation of signaling molecules with consequent effects on development. In that context, enzymatic activities regulating the degree of methyl-esterification of HG are likely to play a major role in the control of plant growth.
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THE METHYL-ESTERIFICATION STATUS OF HG IS CONTROLLED BY PMEs |
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As mentioned above, HG is exported to the cell wall in a fully methyl-esterified form. A defect in galacturonosyl transferase or pectin methyl-transferase activity does not affect the methylation degree of homogalacturonan (Mouille et al., 2007). However, the work of Pereira et al. (2006) suggests that the control of the pool of S-Adenosyl-Methionine may affect the pattern of pectin methyl-esterification. Despite this result, it is well accepted that the methylation status of pectin is mainly controlled by cell wall-localized esterases.
Within the cell wall, HG is modified locally, most notably by removal of methyl groups from the chain, leading to free carboxyl groups and the release of methanol and protons (see Supplemental Figure 1). This reaction is catalyzed by a large family of pectin modifying enzymes called pectin methyl-esterases (PMEs, E.C. 3.1.1.11 [EC] ), belonging to CAZy class 8 of carbohydrate esterases (CE8, www.cazy.org, Cantarel et al., 2009). Depending on primary structure, and the presence of an N-terminal extension (PRO region) preceding the active part (PME domain, Pfam01095), two types of PMEs can be distinguished. Group 1/type II PMEs are characterized by the absence of this PRO region, which shows significant similarity to PMEI proteins (PME Inhibitor domain, PF04043), while group 2/type I PMEs are characterized by the presence of one to three PMEI domains (Pelloux et al., 2007 for review on the PMEs structural motifs). The processing and the role of the PRO region will be discussed below. PME activity, which catalyzes the de-methyl-esterification of the C6-linked methyl-ester groups of HG and produces negative charges, is tightly regulated by endogenous inhibitor proteins called pectin methyl-esterase inhibitors (PMEIs) (Juge, 2006; Pelloux et al., 2007). To date, the mode of action of PMEs on HG remains controversial and seems influenced by a wide range of factors including cell wall pH and the pattern/degree of methyl-esterification of homopolygalacturonic acids. So far, in solution, both random (non-blockwise) and linear (blockwise) PME-mediated de-methyl-esterification patterns of HG were shown (Catoire et al., 1998; Denès et al., 2000; Kim et al., 2005; see Supplemental Figure 1). In Arabidopsis, recent data showed that one heterologously expressed PME isoform was likely to have a blockwise pattern of de-methyl-esterification (Dedeurwaerder et al., 2008). The current lack of information concerning the precise characterization of the biochemical activity of PMEs is related both to the difficulty of expressing the proteins in heterologous system and to the potential redundancy of isoforms. Unraveling the mode of action of PMEs on homogalacturonan is, from our point of view, one of the main current challenges in the field. Determining the substrate specificity and the action pattern of individual PME isoforms will allow linking the enzymes to their effects on pectin structure and properties.
Analysis of genomic data showed that PMEs and PMEIs belong to large multigene families in all plant species analyzed (www.cazy.org; www.tigr.org/tdb/e2k1/ath1; www.arabidopsis.org). For instance, in Arabidopsis thaliana, 66 and 69 ORFs have been annotated as putative full-length PMEs and PMEIs, respectively. Overall, the number of PME and PMEI isoforms appears to be lower in monocotyledonous (Oryza sativa and Brachypodium distachyon) compared to dicotyledonous species (Arabidopsis thaliana and Populus trichocarpa) (Pelloux et al., 2007). In Oryza, figures are 35 and 25, respectively, which is sustained by recent data on Brachypodium (29 PMEs and 38 PMEIs; www.brachybase.org). Considering these data, and although HGs are known to be less abundant in grasses, their modification by PME and PMEIs is likely to play a substantial role in plant development in such species.
Overall, the large number of PME and PMEI isoforms in plants is likely to reflect the diversity of their role in the modification of the cell wall in various aspects of plant development.
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PMEs AND THEIR INHIBITORS IN PLANT DEVELOPMENT |
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In several plant species, a role for PME-mediated changes in HG has been shown in various vegetative and reproductive developmental processes. As most of these processes were reviewed in a previous publication (Pelloux et al., 2007), the current review mainly focuses on the latest results obtained in Arabidopsis and other dicotyledonous. Indeed, over the past few years, despite the large number of PME isoforms in Arabidopsis (66) and the high degree of co-expression, several loss-of-function phenotypes have been described. Recently, the Arabidopsis PME mutant vanguard1 (vgd1) was isolated (Jiang et al., 2005). The pollen-specific PME isoform VGD1 (At2g47040) is among the most abundant mRNAs in the Arabidopsis pollen transcriptome (Pina et al., 2005); however, mutant pollen showed only an 18% reduction in total PME activity. This relatively small reduction in activity led to unstable pollen tubes when germinated in vitro and a decreased fertilization in vivo. Interestingly, the knockout phenotype could be complemented with an isoform (At2g47030) closely related to VGD1 but not with a construct encoding another, slightly more distant isoform (At3g62170), indicating that different PME isoforms may display different activities and are not redundant (Jiang et al., 2005). Similar, albeit weaker, effects on pollen tube growth have been observed with the NtPPME1 and AtPPME1 mutants in tobacco and Arabidopsis, respectively (Bosch and Hepler, 2006; Tian et al., 2006). Mutation of QUARTET1 (QRT1), a PME expressed in Arabidopsis pollen, and anthers leads to impaired pollen tetrade separation during flower development. QRT1 potentially acts in tandem with QRT3, a polygalacturonase, to degrade de-methyl-esterified homogalacturonan in pollen mother cell primary walls (Rhee et al., 2003; Francis et al., 2006), as PME-mediated de-methyl-esterification is thought to be required to render homogalacturonan susceptible to polygalacturonase-mediated degradation (Wakabayashi et al., 2000, 2003). Antisense expression of a root cap-specific PME cDNA in pea (Pisum sativum) resulted in stunted root growth, altered cell shape, and a defect in root border cell separation, emphasizing the critical role of PME activity for adhesion (Wen et al., 1999). More surprisingly, PME appears to be an important enzyme in stabilizing pectins during wood formation. In aspen trees, PttPME1 is notably involved in the regulation of fiber length by strengthening cellular adhesion between developing fibers, and thus inhibiting their intrusive apical elongation (Siedlecka et al., 2008). In potato (Solanum tuberosum), antisense expression-mediated decrease in PME activity led to stunted growth, an altered leaf growth pattern, and changed ion content of the cell walls (Pilling et al., 2004).
Strikingly, a recent study showed that PME activity could induce primordia formation and override primordia patterning in Arabidopsis inflorescence meristems. Conversely, overexpression of a PMEI completely prevents formation of lateral organs, highlighting the importance of regulated pectin de-methyl-esterification for plant development (Peaucelle et al., 2008). Whether the impact of PME/PMEI activity on primordia formation occurs through direct effect on the mechanical properties of the cell wall or indirect effect through the release of OGA and/or regulation of the efflux of auxin remain major questions for future research.
In addition to its roles in development, PME seems to be involved in plant–pathogen interactions. It has been reported that PME is a host receptor for the tobacco mosaic virus (TMV) movement protein. Accordingly, silencing of PME expression leads to diminished systemic movement of TMV (Dorokhov et al., 1999; Chen et al., 2000; Chen and Citovsky, 2003). Moreover, AtPME3 from Arabidopsis seems to interact with the cellulose binding protein of the cyst nematode Heterodera schachtii and enhances plant susceptibility to this pathogen (Hewezi et al., 2008). The degree and the pattern of methyl-esterification of HG mediated by PMEs are important determinants of the biological activity of oligogalacturonides, leading to the elicitation of plant defense responses (Osorio et al., 2008). The role of the fine tuning of the degree of HG methyl-esterification during plant–pathogen interactions can further be illustrated by results concerning the restriction of fungal infection by Botrytis in Arabidopsis plants overexpressing two PMEIs (At1g48020 and At3g17220) (Lionetti et al., 2007).
PMEIs, first purified from kiwi fruit (Camardella et al., 2000), show strong similarity with invertase inhibitors (INH), although their respective target enzymes are unrelated (Rausch and Greiner, 2004). PMEI-related proteins were subsequently identified as multigenic families in several species including Arabidopsis (69 members), but, so far, studies describing their roles in plant development are scarce. However, it is likely that the specific co-regulation and interaction of given PME and PMEI isoforms, as suggested in recent studies, are of the utmost importance in controlling the degree of methyl-esterification of pectins and thus modifying cell wall mechanical properties during growth (Röckel et al., 2008; Peaucelle et al., 2008).
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TRANSCRIPTIONAL REGULATION OF PME AND PMEI |
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The analysis of transcriptomic data suggests that expression of PME and PMEI is indeed highly correlated in various tissues and developmental stages in Arabidopsis. Co-expressed PME and PMEI transcripts have notably been identified during secondary growth (Ko et al., 2004), in the xylem/phloem complex (Zhao et al., 2005), in pollen (Pina et al., 2005), as well as more recently in developing stems (Minic et al., 2009). In dark-grown hypocotyls, for which it is known that control of the degree of HG methyl-esterification might be crucial for development (Derbyshire et al., 2007), results obtained at the transcriptome level were validated at the proteome level (Irshad et al., 2008). Such potential specificity of PME–PMEI isoforms can further be illustrated by the identification of two PMEs preferentially interacting with AtPMEI-1 and AtPMEI-2 in leaves of Arabidopsis (Lionetti et al., 2007). Cluster analysis of publicly available microarray data for one-third of the PME and PMEI gene family show five distinct expression clusters, each of which containing several PME and PMEI isoforms (Figure 1). The specificity of the localization of transcript expression (seed coat, shoot apex, micropylar endosperm, chalazal endosperm, pollen for expression cluster 1 to 5, respectively) would suggest that specific interaction of given PME and PMEI isoforms is a key determinant of the localized modification of HG methyl-esterification status during development. For expression clusters 2 and 5, transcript expression patterns are related to similar activities of the promoter in the shoot apex and in pollen grain, respectively. A striking role of the PME and PMEI isoforms of these two clusters was recently shown (Röckel et al., 2008; Peaucelle et al., 2008).
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REGULATION OF PMEs BY ENDOCYTOSIS OF PMEIs |
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Based on the strong effects of the biochemically characterized inhibitor isoforms on PME activity (Camardella et al., 2000; D'Avino et al., 2003; Wolf et al., 2003; Raiola et al., 2004), PMEIs are assumed to provide an effective post-translational control mechanism. Accordingly, ectopic expression of two Arabidopsis pollen PMEIs resulted in silencing of PME activity in transgenic plants that were, as a result, more resistant to Botrytis infection (Lionetti et al., 2007). Recently, a meristem-expressed PMEI was used as an effective tool to decrease PME activity in meristems, which resulted in the suppression of lateral organ formation (Peaucelle et al., 2008). However, the physiological role of the interplay of PMEIs with PMEs is far from clear and, to date, only one loss-of-function effect of any PMEI protein has been shown. CaPMEI1 from pepper (Capsicum annuum L.) shows antifungal activities and CaPMEI1 expression is induced after challenge with Xanthomonas campestris pv. vesicatoria. Consequently, after virus-induced gene silencing of CaPMEI1, pepper plants were more susceptible to attack of this pathogen (An et al., 2008).
In order to shed light on the role of the PME–PMEI interaction, the pollen tube, at present, represents one of the best available systems because (1) regulated pectin modification is essential for pollen tube growth, (2) both PMEs and PMEIs are highly expressed in pollen, and (3) the pollen tube is a simple experimental system amenable to advanced in vivo imaging techniques (Bosch et al., 2005; Bosch and Hepler, 2005; Jiang et al., 2005; Parre and Geitmann, 2005a; Pina et al., 2005; Bosch and Hepler, 2006; Tian et al., 2006).
Through the use of pectin-specific antibodies, a remarkable distribution of HG epitopes with different degrees of methylesterification has been demonstrated in the pollen tube. At the growing tip region, the HG is partially methyl-esterified, which was demonstrated by labeling with the JIM7 antibody. On the other hand, HG with a lower level of methyl-esterification is observed in the pollen tube shank (Figure 2A), as indicated by labeling with the JIM5 antibody (Bosch et al., 2005; Parre and Geitmann, 2005b), which optimally binds to at least four unesterified residues flanked by residues with methylesters (Clausen et al., 2003). The maintenance of this distribution is essential for pollen tube growth, as premature de-methyl-esterification of the tip region through exogenous supply of PME was shown to block tube elongation (Bosch et al., 2005; Parre and Geitmann, 2005b). Apparently, JIM7 epitopes are substrates of PME, and JIM5 epitopes are reaction products, as the above-mentioned incubation with PME resulted in the increase of JIM5 labeling at the tip and the complete absence of JIM7 labeling (Parre and Geitmann, 2005b). Confocal microscopy analysis of living pollen tube revealed that AtPMEI-2, a pollen-specific PMEI from Arabidopsis, localizes exclusively to the pollen tube tip, whereas AtPPME1, a PME interacting with AtPMEI-2, is present both at the tip and the flanks of the tube (Röckel et al., 2008). The tip-restricted localization of the PMEI protein seems to be maintained by selective endocytosis, as AtPMEI-2 was shown to be trapped in BFA-induced endosomal aggregates whereas AtPPME1 localization was unaffected by BFA treatment. Similar results were observed when formation of endosomal aggregates was provoked by overexpression of a FYVE-domain protein, which binds to and sequesters phosphatidylinositol-3-phosphate enriched endosomal membranes (Röckel et al., 2008). There are at least two different endocytic mechanisms operative in the pollen tube. At the extreme apex, so-called smooth (clathrin-independent) endocytosis leads to a coned-shaped zone of endocytic vesicles, which can be easily recognized by lipophilic tracer dyes such as FM4-64. In addition, clathrin-mediated endocytosis takes place in the sub-apical region (Moscatelli et al., 2007; Bove et al., 2008).
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These observations suggest that endocytic uptake of AtPMEI-2 at the flanks of the pollen tube mediates the tip-restricted localization of this protein. Notably, the observed sub-cellular localization of PMEI and PME together with the selective endocytosis of the inhibitor would provide a mechanism for the maintenance of the unique pectin distribution in pollen tubes (Figure 2A). However, it remains to be demonstrated how dissociation of the rather stable PME–PMEI complex is mediated.
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REGULATION OF TRAFFICKING AND PROCESSING OF GROUP2/TYPE I PMEs: THE ROLE OF SUBTILISIN |
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Interestingly, the majority of PME isoforms (group II/type I) features an N-terminal domain, the PRO region, which displays similarity with PMEIs and therefore has been suspected to constitute an autoinhibitory domain that must be proteolytically released to enable PME activity. While biochemical analysis of recombinantly expressed PRO region protein failed to support an inhibitory role, evidence has been provided for an involvement of this N-terminal domain in sub-cellular targeting (Bosch et al., 2005; Dorokhov et al., 2006). Expression of an N-terminal truncation of NtPPME1, a pollen-specific group II PME from tobacco, resulted in reduced growth, despite an apparent loss of the extracellular targeting of NtPPME1, indicating that intracellular pectin de-methyl-esterification is detrimental to the cell. This detrimental effect could be explained either by direct changes in wall properties or by intracellular sequestration of pectin-binding proteins. Interestingly, co-expression of the PRO region partially restored extracellular targeting (Bosch et al., 2005). However, experiments performed with the GFP-tagged version of the tobacco PME proPME-1 suggested that only the N-terminal transmembrane domain present in this PME is necessary to mediate apoplastic targeting, as the PMEI-homologous domain could be deleted without change of localization (Dorokhov et al., 2006). Through differential extraction of cell wall and intracellular proteins, respectively, the same study provided evidence for a proPME-1 processing event inside of the cell or immediately after release into the apoplast (Dorokhov et al., 2006). Recently, it was demonstrated that proteolytic release of the PRO region at two basic motifs located between PRO region and catalytic domain of group II PMEs occurs in the Golgi apparatus and is a prerequisite for apoplastic targeting of the PME domain (Wolf et al., 2009). Interestingly, the two basic cleavage motifs, which display the consensus sequence RKLL, are also observed in substrate proteins of the mammalian site-1 protease (Toure et al., 2000). Analysis of an insertion mutant of AtS1P, the Arabidopsis ortholog of site-1 protease, demonstrated an impaired PME processing and thus an involvement of subtilisin-like protease in PME maturation. AtS1P shows moderate but ubiquitous expression based on publicly available microarray data. Notably, mRNA levels do not seem to be affected considerably by any biotic or abiotic treatment (www.genevestigator.ethz.ch). It is an appealing possibility that processing could be regulated on the post-translational level, enabling controlled activation and transport of group II PMEs in a single step. One conceivable purpose of this regulation mechanism could be the coordination of PME maturation with HG biosynthesis and methyl-esterification, which also take place in the Golgi apparatus (Figure 2B).
Presumably, other proteases besides AtS1P are involved in PME maturation, as the processing in s1p mutant plants was only impaired rather than completely prevented (Wolf et al., 2009). The identification of additional proteases as well as other putative factors involved in PME processing and/or Golgi retention is clearly one of the most urgent challenges ahead.
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OUTLOOK |
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Over the past few years, functional genomics approaches have generated a fair amount of data demonstrating the major role of the control of the HG methyl-esterification in several developmental processes. In that context, the function and regulation of pectin methyl-esterases have been primarily investigated, shedding new light on the diversity of the roles of the proteins. For instance, a key role for PMEs and PMEIs in controlling the degree of methyl-esterification of HG within the apical meristem was shown (Peaucelle et al., 2008). This result opens exciting new perspectives to discriminate between signaling (auxin or OGA-related) and mechanical events involved in the process of primordia emergence. The intricate relations between PMEs and PMEIs during pollen tube growth were investigated, showing a surprising regulation of PME by endocytosis of PMEIs (Röckel et al., 2008). In addition, much progress has been made in discovering the key events involved in the processing of the PRO part of group 2 PME proteins and discovering the role of subtilases (Wolf et al., 2009). This result brought, at last, some solid information on the much discussed targeting of PME proteins, and an explanation for the occurrence of solely the mature part of the proteins in the cell wall. Altogether, if exciting perspectives are emerging for the role of PME/PMEI-mediated de-methyl-esterification of HG in plant development, major bottlenecks are still ahead. In particular, and although experimental work in controlled conditions is emerging (Slavov et al., 2009), the way PME activities influence the fine structure of HG and therefore its rheological properties in the context of the plant cell wall are still to be solved. There is currently an urgent need for generating data on the mode of action of PMEs (substrate and pH specificity, de-methyl-esterification pattern). This is of the utmost importance in order to understand the diverse roles of PME isoforms in Arabidopsis and other plants. This, together with detailed spatial and temporal analysis of pectic epitopes, will help linking one given isoform to a specific change in HG structure that could specifically impact on cell wall rheology and thus plant development. In this respect, it is necessary that the existing HG antibodies are characterized further and desirable that novel ones specific for certain methylation patterns are generated. Further need in this field of research is to relate a specific PMEI to its specific PME counterparts. Considering the co-expression of PME and PMEI isoforms, it is likely that the relative PME and PMEI protein levels are a key regulating point of changes in HG methyl-esterification status. A large-scale protein–protein interaction approach could help in revealing specific interacting PME–PMEIs.
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SUPPLEMENTARY DATA |
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Supplementary Data are available at Molecular Plant Online. No conflict of interest declared.
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