Homogalacturonan-modifying enzymes: structure, expression, and roles in plants

Abstract

Understanding the changes affecting the plant cell wall is a key element in addressing its functional role in plant growth and in the response to stress. Pectins, which are the main constituents of the primary cell wall in dicot species, play a central role in the control of cellular adhesion and thereby of the rheological properties of the wall. This is likely to be a major determinant of plant growth. How the discrete changes in pectin structure are mediated is thus a key issue in our understanding of plant development and plant responses to changes in the environment. In particular, understanding the remodelling of homogalacturonan (HG), the most abundant pectic polymer, by specific enzymes is a current challenge in addressing its fundamental role. HG, a polymer that can be methylesterified or acetylated, can be modified by HGMEs (HG-modifying enzymes) which all belong to large multigenic families in all species sequenced to date. In particular, both the degrees of substitution (methylesterification and/or acetylation) and polymerization can be controlled by specific enzymes such as pectin methylesterases (PMEs), pectin acetylesterases (PAEs), polygalacturonases (PGs), or pectate lyases-like (PLLs). Major advances in the biochemical and functional characterization of these enzymes have been made over the last 10 years. This review aims to provide a comprehensive, up to date summary of the recent data concerning the structure, regulation, and function of these fascinating enzymes in plant development and in response to biotic stresses.

Understanding plant cell-wall remodelling during the symbiotic interaction between Tuber melanosporum and Corylus avellana using a carbohydrate microarray

“…Although our data underline a difficulty in the interpretation of the results due to the presence of both fungal and plant cell-wall components, a localized degradation of HG (the most abundant plant pectin polymer) can be suggested during fungal colonization, in agreement with the growth of the colonizing fungus through the middle lamella and the fungal gene expression of genes acting on these polysaccharides. Understanding HG remodelling by specific fungal or plant enzymes, and how these changes are spatially and temporally mediated, is a central issue in addressing the fundamental role of HGtype pectins during plant growth and in plant response to environmental changes (Sénéchal et al 2014). Considering the role of de-methylesterified HG-derived oligogalacturonides (OGs) as signalling molecules (Ferrari et al 2013), the present findings raise the question of whether HG hydrolysis can act as a source of pectin fragments that are capable of eliciting plant responses during ectomycorrhizal symbiosis.…”

PECTIN METHYLESTERASE48 Is Involved in Arabidopsis Pollen Grain Germination

“…As discussed by Jolie et al (2010), the pH, the DM, and the pattern of methylesterification are known to modify the mode of action of PMEs (Catoire et al, 1998;Denès et al, 2000;Sénéchal et al, 2014). Thus, we can also hypothesize that, upon random action of the PME (PME48 or others from the 13 other pollen-specific PMEs), the partial removal of methylester groups may allow other pectin-degrading enzymes such as PGases and/or PLs to cleave the HG, affecting the rigidity of the cell wall (Micheli, 2001;Sénéchal et al, 2014).…”

“…Thus, we can also hypothesize that, upon random action of the PME (PME48 or others from the 13 other pollen-specific PMEs), the partial removal of methylester groups may allow other pectin-degrading enzymes such as PGases and/or PLs to cleave the HG, affecting the rigidity of the cell wall (Micheli, 2001;Sénéchal et al, 2014). In the Arabidopsis genome, 69 annotated genes can be classified as putative PGases (González-Carranza et al, 2007).…”

“…In that case, demethylesterified HG can form ionic bonds between the negatively charged carboxyl groups of several HG chains and Ca 2+ ions, forming a pectate gel that may provide sufficient stiffness to the pollen tube cell wall (Micheli, 2001;Geitmann and Steer, 2006;Chebli et al, 2012). Alternatively, the partial removal of noncontiguous methylester groups by PMEs, which is named the random mode of action, may allow pectindegrading enzymes (such as polygalacturonases [PGases] and pectate lyases [PLs]) to cleave the HG backbone, thus affecting the rigidity of the cell wall (Micheli, 2001;Parre and Geitmann, 2005a;Sénéchal et al, 2014). Therefore, the fine control of the modulation of the degree of methylesterification (DM) of the HG by PMEs is of main importance (Wolf et al, 2009a) in the pollen tube growth dynamics.…”

Glycoside Hydrolases in Plant Cell Wall Proteomes: Predicting Functions That Could Be Relevant for Improving Biomass Transformation Processes

“…Glycosidases and glycanases have exo-and endo-GH activities, respectively, while trans-glycosidases and transglycanases perform exo-and endo-transglycosylation, respectively. Pectin methylesterases and pectin acetylesterases control the degree of homogalacturonan methylesterification and acetylation, respectively [15]. Class III peroxidases (Prxs) can either form covalent bonds by oxidizing aromatic compounds such as monolignols or aromatic amino acids or produce reactive oxygen species that participate in non-enzymatic breakage of covalent bonds of polysaccharides [16].…”