Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion.
Homogalacturonan (HG) is a multifunctional pectic polysaccharide of the primary cell wall matrix of all land plants. HG is thought to be deposited in cell walls in a highly methyl-esterified form but can be subsequently de-esterified by wall-based pectin methyl esterases (PMEs) that have the capacity to remove methyl ester groups from HG. Plant PMEs typically occur in multigene families/isoforms, but the precise details of the functions of PMEs are far from clear. Most are thought to act in a processive or blockwise fashion resulting in domains of contiguous de-esterified galacturonic acid residues. Such de-esterified blocks of HG can be cross-linked by calcium resulting in gel formation and can contribute to intercellular adhesion. We demonstrate that, in addition to blockwise de-esterification, HG with a non-blockwise distribution of methyl esters is also an abundant feature of HG in primary plant cell walls. A partially methyl-esterified epitope of HG that is generated in greatest abundance by non-blockwise de-esterification is spatially regulated within the cell wall matrix and occurs at points of cell separation at intercellular spaces in parenchymatous tissues of pea and other angiosperms. Analysis of the properties of calcium-mediated gels formed from pectins containing HG domains with differing degrees and patterns of methyl-esterification indicated that HG with a non-blockwise pattern of methyl ester group distribution is likely to contribute distinct mechanical and porosity properties to the cell wall matrix. These findings have important implications for our understanding of both the action of pectin methyl esterases on matrix properties and mechanisms of intercellular adhesion and its loss in plants.
Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
W G
WG
Willats
C
C
Orfila
G
G
Limberg
H C
HC
Buchholt
G J
GJ
van Alebeek
A G
AG
Voragen
S E
SE
Marcus
T M
TM
Christensen
J D
JD
Mikkelsen
B S
BS
Murray
J P
JP
Knox
D000911:Antibodies, Monoclonal / Q000378:metabolism; D001667:Binding, Competitive; D002118:Calcium / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism; D002473:Cell Wall / Q000737:chemistry*; D004305:Dose-Response Relationship, Drug; D004797:Enzyme-Linked Immunosorbent Assay; D000939:Epitopes; D004951:Esterification; D007150:Immunohistochemistry; D008954:Models, Biological; D018532:Pisum sativum / Q000737:chemistry*; D010368:Pectins / Q000737:chemistry*; D010940:Plant Proteins / Q000378:metabolism; D011096:Polygalacturonase / Q000378:metabolism; D011133:Polysaccharide-Lyases / Q000378:metabolism; D017434:Protein Structure, Tertiary; D013997:Time Factors
D000911:Antibodies, Monoclonal; D000939:Epitopes; D010940:Plant Proteins; D010368:Pectins; C400187:endopolygalacturonase II; D011096:Polygalacturonase; D011133:Polysaccharide-Lyases; C027349:pectin lyase; D002118:Calcium; C003181:polygalacturonic acid