Abstract
Summary Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure–function relationships of the plant cell wall, it is imperative to trace the origin of its different components.The present study is focused on plant 1,4‐β‐xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and algae. It substantiates the findings by heterologous expression and biochemical characterization of a charophyte alga xylan synthase.Of the 12 known gene classes involved in 1,4‐β‐xylan formation, XYS1/IRX10 in plants, IRX7, IRX8, IRX9, IRX14 and GUX occurred for the first time in charophyte algae. An XYS1/IRX10 ortholog from Klebsormidium flaccidum, designated K. flaccidum XYLAN SYNTHASE‐1 (Kf XYS1), possesses 1,4‐β‐xylan synthase activity, and 1,4‐β‐xylan occurs in the K. flaccidum cell wall.These data suggest that plant 1,4‐β‐xylan originated in charophytes and shed light on the origin of one of the key cell wall innovations to occur in charophyte algae, facilitating terrestrialization and emergence of polysaccharide‐based plant cell walls.
Highlights
A large diversity of cell wall structural variations exist within the plant kingdom (Domozych et al, 2007; Harholt et al, 2012)
We demonstrated xylan synthase activity for one of the members of the earliest xylan synthesis-specific gene homologs identified to date: a K. flaccidum IRX10/XYLAN SYNTHASE-1 (XYS1) ortholog (Kf XYS1)
Evolutionary appearance of genes involved in xylan biosynthesis
Summary
A large diversity of cell wall structural variations exist within the plant kingdom (Domozych et al, 2007; Harholt et al, 2012). It is clear that some cell wall functions can be fulfilled by different architectural solutions, for example involving different groups of polysaccharides (Carpita & Gibeaut, 1993; Harholt et al, 2012). This suggests that simple carbohydrate composition gives a limited perspective of wall structure, whereas the combinatorial aspects of polymer–polymer interactions are the key players that define architectural complexity. Before we can answer these questions it is necessary to establish the key routes of cell wall evolution by determining the evolutionary origins of the different cell wall polysaccharide classes to fill in current gaps in our knowledge
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