A review of xylan and lignin biosynthesis: Foundation for studying Arabidopsisirregular xylemmutants with pleiotropic phenotypes

Abstract

Plant cells are surrounded by a carbohydrate-rich extracellular matrix known as the cell wall. Primary cell walls are laid down around dividing and elongating cells and consist largely of the polysaccharides cellulose, hemicelluloses, and pectin along with approximately 10% protein. Specific cells such as xylem vessels and fibers lay down a secondary wall rich in cellulose, hemicellulose, and lignin, with lesser amounts of pectin. Most of the models depict the plant cell wall as a matrix of separate polysaccharides. However, the recent identification of a proteoglycan that contains covalently attached pectin and xylan indicates that at least some of these wall glycans exist as domains within a single glycopolymer and that current models of the wall need to be revised. Furthermore, several cell wall biosynthesis mutants, including the secondary cell wall mutant irregular xylem (irx) 8, are affected in multiple cell wall polymers making it challenging to define the biochemical function of the mutated gene. The goal of this review is to provide a background for studying genes which encode secondary cell wall biosynthetic proteins whose mutation affects multiple wall polymers including xylan and lignin. We first review the phenotypes of the irx mutants and then summarize the current understanding of the structure and synthesis of xylan and lignin along with a review of transcription factors known to affect secondary wall synthesis. This review is intended to serve as a resource for those studying genes that encode proteins involved in the synthesis of plant secondary wall lignin and xylan.

Asparagus IRX9, IRX10, and IRX14A Are Components of an Active Xylan Backbone Synthase Complex that Forms in the Golgi Apparatus

“…2). This may be due to IRX10 functional variations between plant species and/or differences in the heterologous expression systems (for review, see Hao and Mohnen, 2014). Similarly, expression of AoIRX14A also was capable of adding a single Xyl residue to the Xyl 5 -AA acceptor.…”

“…Additionally, the reducing end (RE) sequence of heteroxylans from dicots and gymnosperms differs from that of grasses. In the dicots/gymnosperms, it is a characteristic tetrasaccharide glycosyl sequence, b-D-Xylp-(1→3)-a-L-Rhap-(1→2)-a-D-GalpA-(1→4)-D-Xylp, that is absent in the grasses (for review, see Hao and Mohnen, 2014). Recently, Ratnayake et al (2014) reported that the RE glycosyl sequence of wheat (Triticum aestivum) endosperm arabinoxylan constitutes a linear (1→4)-b-DXylp backbone that may be monosubstituted either with an a-L-Araf residue at the RE b-D-Xylp residue and/or the penultimate RE b-D-Xyl residue or with an a-D-GlcpA residue at the RE b-D-Xylp residue.…”

“…Orthologs of the AtIRX proteins have been identified in many other species, including wheat (Zeng et al, 2010), Populus trichocarpa (Lee et al, 2012b), Physcomitrella patens (Hörnblad et al, 2013), Plantago ovata (Jensen et al, 2013), rice (Oryza sativa; Chen et al, 2013;Chiniquy et al, 2013), Gossypium hirsutum , Neolamarckia cadamba (Zhao et al, 2014), and garden asparagus (Asparagus officinalis; Song et al, 2015). Enzymes involved in xylan backbone biosynthesis as well as side chain decorations, such as the arabinosyltransferases, glucuronosyltransferases, and acetylation enzymes, were recently reviewed by Rennie and Scheller (2014) and Hao and Mohnen (2014).…”

Role of Glycosyltransferases in Pollen Wall Primexine Formation and Exine Patterning

“…Similarly, the paralogs IRX14 and IRX14L also encode members of the GT43 family. IRX9 and IRX14 play major, nonredundant roles in xylan backbone elongation required for GX biosynthesis (Hao and Mohnen, 2014), although their presumed functions as xylan:xylosyltransferases with GT enzymatic activity has recently been called into question (Ren et al, 2014). Genetic evidence suggests that IRX9 and its paralog IRX9L, as well as IRX14 and its paralog IRX14L, encode pairs of proteins with the same functions in the biosynthesis of the xylan backbone (Lee et al, 2011;Keppler and Showalter, 2010;Wu et al, 2010).…”

“…Arabidopsis mutants defective in xylan biosynthesis typically exhibit irx phenotypes characterized by collapsed vessel elements (Hao and Mohnen, 2014), which suggests a key role for GX in secondary cell wall structure and function. The SPG2 locus, identified by its spg exine patterning phenotype (Dobritsa et al, 2011) is synonymous to IRX9L, which, like IRX9, encodes a member of the GT43 family of GTs (Peña et al, 2007;Wu et al, 2010).…”