Modern mannan: a hemicellulose's journey

Abstract

Summary Hemicellulosic polysaccharides built of β‐1,4‐linked mannose units have been found throughout the plant kingdom and have numerous industrial applications. Here, I review recent advances in the biosynthesis and modification of plant β‐mannans. These matrix polymers can associate with cellulose bundles to impact the mechanical properties of plant fibers or biocomposites. In certain algae, mannan microfibrils even replace cellulose as the dominant structural component of the cell wall. Conversely, patterned galactoglucomannan found in Arabidopsis thaliana seed mucilage significantly modulates cell wall architecture and abiotic stress tolerance despite its relatively low content. I also discuss the subcellular requirements for β‐mannan biosynthesis, the increasing number of carbohydrate‐active enzymes involved in this process, and the players that continue to be puzzling. I discuss how cellulose synthase‐like enzymes elongate (gluco)mannans in orthogonal hosts and highlight the discoveries of plant enzymes that add specific galactosyl or acetyl decorations. Hydrolytic enzymes such as endo‐β‐1,4‐mannanases have recently been involved in a wide range of biological contexts including seed germination, wood formation, heavy metal tolerance, and defense responses. Synthetic biology tools now provide faster tracks to modulate the increasingly‐relevant mannan structures for improved plant traits and bioproducts.

Branched mannan and xyloglucan as a dynamic duo in plant cell walls

“…While β-mannans likely represent the most ancient hemicellulose in the plant kingdom, XyG emerged as the dominant hemicellulose in the PCWs of most angiosperms ( Scheller and Ulvskov, 2010 ). Nevertheless, in some walls such as the softwood of gymnosperms, GGM accumulates as the most abundant hemicellulose after cell expansion is completed ( Voiniciuc, 2022 ). In Arabidopsis thaliana (Arabidopsis hereafter), five CELLULOSE SYNTHASE-LIKE C ( CSLC ) genes are functionally redundant for the elongation of XyG ( Kim et al, 2020 ), while at least four of the nine CELLULOSE SYNTHASE-LIKE A ( CSLA ) genes encode (gluco)mannan synthases ( Voiniciuc, 2022 ).…”

“…Nevertheless, in some walls such as the softwood of gymnosperms, GGM accumulates as the most abundant hemicellulose after cell expansion is completed ( Voiniciuc, 2022 ). In Arabidopsis thaliana (Arabidopsis hereafter), five CELLULOSE SYNTHASE-LIKE C ( CSLC ) genes are functionally redundant for the elongation of XyG ( Kim et al, 2020 ), while at least four of the nine CELLULOSE SYNTHASE-LIKE A ( CSLA ) genes encode (gluco)mannan synthases ( Voiniciuc, 2022 ). Plant β-1,4-glucan or mannan polymers can be elongated in yeast using CSLC ( Cocuron et al, 2007 , Robert et al, 2021 ) or CSLA expression ( Robert et al, 2021 , Voiniciuc et al, 2019 ), respectively.…”

“…Mannanase digestion released only trace amounts of carbohydrates from the csla2 csla9 double mutant. This suggests that there may be a functional and tissue-dependent specialization within the CSLA family, but raises new questions about the roles of other CSLAs in Arabidopsis ( Voiniciuc, 2022 ). The latest data show that CSLA9 -dependent acetylated glucomannan motifs are found in PCW-rich tissues such as leaves ( Yu et al, 2022 ), while CSLA2 is required for repeating Glc-Man domains regularly substituted Gal side chains (discussed in next section).…”

“…The backbones of mannans and XyG can be substituted by GT34 enzymes with α-1,6-linked Gal or xylosyl (Xyl), respectively, or can be O -acetylated at the C-2 and C-3 positions ( Pauly and Keegstra, 2016 , Voiniciuc, 2022 ). Single α-1,6-Gal units are attached to Man by MANNAN α-GALACTOSYLTRANSFERASE1/MUCILAGE-RELATED 10 (MAGT1/MUCI10) using UDP-Gal ( Voiniciuc et al, 2015b , Yu et al, 2018 ), while XyG Xyl TRANSFERASES (XXT) use UDP-Xyl as to add regular patterns in vivo ( Culbertson et al, 2018 ).…”

“…(Gluco)mannan backbones are built of β-1,4-mannosyl (Man) units, sometimes interspersed with β-1,4-glucosyl (Glc) units, while XyG backbone is built exclusively of β-1,4-Glc. The biosynthesis of conserved XyG branches has been extensively investigated by several research groups (reviewed by Julian and Zabotina, 2022 ), but plant β-mannans appeared to be composed of irregularly distributed glycosidic residues until recently (reviewed by Voiniciuc, 2022 ). Subsequently, Yu et al (2022) identified a patterned galactoglucomannan (GGM) containing repeating Glc-Man backbone units and regularly spaced β-Gal-α-Gal disaccharide side chains.…”