Polysaccharides tightly retained by cellulose in collenchyma and xyloglucan-depleted parenchyma cell walls

Cellulose microfibrils in plant cell walls are embedded within a matrix of non-cellulosic polysaccharides, whose interactions critically influence cell wall mechanics, function, and processing of plant raw materials. This study provides the first comparative analysis of cellulose retained polysaccharides in primary cell walls of celery petiole collenchyma and parenchyma, two tissues differing in wall thickness, microfibril organization, and function. Using selective cellulose dissolution (DMAc-LiCl, MMNO) combined with cellulase treatment and comprehensive compositional, molecular weight, and structural analyses, we characterized polysaccharides tightly retained by cellulose. Collenchyma cell walls exhibited higher levels of tightly retained polysaccharides, consistent with highly ordered microfibrils with aggregated contact zones. Pectins, predominantly rhamnogalacturonan I and homogalacturonan, were major components in both tissues; collenchyma pectins were enriched in branched β-(1,4,6)-galactans, while parenchyma pectins had more branched α-(1,3,5)-arabinans. Most homogalacturonan was extremely tightly bound to cellulose in both tissues. Low-molecular weight arabinose-rich polysaccharides likely mediate cellulose-pectin interactions, possibly substituting for xyloglucan, which is at a lower level in these walls and minimal for parenchyma walls. Hemicelluloses (xyloglucan, xylan, mannan), were present at lower levels, with one pool of mannans effectively released by DMAc penetrating into cellulose microfibrils from the non-reducing ends. These findings reveal tissue-specific polysaccharide combinations tightly integrated with cellulose microfibrils, underpinning differences in cell wall architecture, mechanical properties, and remodeling during growth.