Occurrence of the Primary Cell Wall Polysaccharide Rhamnogalacturonan II in Pteridophytes, Lycophytes, and Bryophytes. Implications for the Evolution of Vascular Plants

Abstract

Borate ester cross-linking of the cell wall pectic polysaccharide rhamnogalacturonan II (RG-II) is required for the growth and development of angiosperms and gymnosperms. Here, we report that the amounts of borate cross-linked RG-II present in the sporophyte primary walls of members of the most primitive extant vascular plant groups (Lycopsida, Filicopsida, Equisetopsida, and Psilopsida) are comparable with the amounts of RG-II in the primary walls of angiosperms. By contrast, the gametophyte generation of members of the avascular bryophytes (Bryopsida, Hepaticopsida, and Anthocerotopsida) have primary walls that contain small amounts (approximately 1% of the amounts of RG-II present in angiosperm walls) of an RG-II-like polysaccharide. The glycosyl sequence of RG-II is conserved in vascular plants, but these RG-IIs are not identical because the non-reducing l-rhamnosyl residue present on the aceric acid-containing side chain of RG-II of all previously studied plants is replaced by a 3-O-methyl rhamnosyl residue in the RG-IIs isolated from Lycopodium tristachyum, Ceratopteris thalictroides, Platycerium bifurcatum, and Psilotum nudum. Our data indicate that the amount of RG-II incorporated into the walls of plants increased during the evolution of vascular plants from their bryophyte-like ancestors. Thus, the acquisition of a boron-dependent growth habit may be correlated with the ability of vascular plants to maintain upright growth and to form lignified secondary walls. The conserved structures of pteridophyte, lycophyte, and angiosperm RG-IIs suggests that the genes and proteins responsible for the biosynthesis of this polysaccharide appeared early in land plant evolution and that RG-II has a fundamental role in wall structure.Plants first colonized the land approximately 480 million years ago. These early land plants, which are believed to be related to extant bryophytes (Kenrick and Crane, 1997;Qiu and Palmer, 1999), subsequently gave rise to the tracheophytes that now dominate the terrestrial environment. Many of the morphological and biochemical changes that allowed plants to adapt to life on land have been documented (Graham, 1993;Niklas, 1997). However, the limited amount of information available on the composition and architecture of non-flowering plant cell walls (Ligrone et al., 2002;Popper and Fry, 2003) is an impediment to understanding the evolutionary origins of cell walls and the changes in wall structure that occurred during the evolution of land plants.All growing plant cells are surrounded by a polysaccharide-rich primary wall. Primary walls regulate cell expansion and also have important roles in plant growth and development, in the defense against micro-organisms (Carpita and Gibeaut, 1993), and in intercellular signaling (Ridley et al., 2001). The primary walls of seed-bearing tracheophytes (gymnosperms and angiosperms) are composed predominantly of cellulose, hemicellulose, and pectin together with lesser amounts of structural glycoproteins, minerals, enzymes, and phenolic esters (Carpita ...

Hormonal regulation in green plant lineage families

“…The genomes of bryophytes have been suggested to be a rich source of novel genes (Matsunaga et al, 2004;Proctor, 2001;Rensing et al, 2002;Wood et al, 1999). Mention may be made of a novel phytochrome gene in the moss Ceratodon purpureus which actually encodes a light regulated protein kinase of 140 kDa (Thummler et al, 1992).…”

How Have Plant Cell Walls Evolved?

“…It is true that in some cases, the appearance of specific cell wall components can be placed in a clear, if sometimes broad, phylogenic contexts and these have been recently reviewed (Popper, 2008;Sarkar et al, 2009). For example, XyG is thought to be restricted to embryophytes (although this is discussed in more detail later) and rhamnogalacturonan II (RGII) is almost exclusively found in vascular plants (Matsunaga et al, 2004;Popper, 2008). RGII levels appear to have generally increased during the evolution of vascular plants, a trend that is probably correlated with upward growth and the ability to form lignified secondary walls (Matsunaga et al, 2004).…”

“…For example, XyG is thought to be restricted to embryophytes (although this is discussed in more detail later) and rhamnogalacturonan II (RGII) is almost exclusively found in vascular plants (Matsunaga et al, 2004;Popper, 2008). RGII levels appear to have generally increased during the evolution of vascular plants, a trend that is probably correlated with upward growth and the ability to form lignified secondary walls (Matsunaga et al, 2004). RGII can be cross-linked by boron, and it is significant that grasses, which have a lower requirement for boron than dicots, also have reduced levels of RGII in their walls.…”

Arabidopsis thaliana RGXT1 and RGXT2 Encode Golgi-Localized (1,3)-α-d-Xylosyltransferases Involved in the Synthesis of Pectic Rhamnogalacturonan-II

“…RG-II consists of 12 different glycosyl residues, including the rare sugars, D-apiose (D-Api), L-aceric acid (3-Ccarboxy-5-deoxy-L-xylose), 2-O-methyl L-fucose, 2-O-methyl D-xylose (2-O-Me-D-Xyl), L-galactose, 3-deoxy-D-lyxo-heptulosaric acid, and 3-deoxy-D-manno-oct-2-ulosonic acid, linked together by no less than 22 different glycosidic linkages. The structure of RG-II is highly conserved in all vascular plants examined to date, while lower land plants appear to have a 100-fold lower content of a polysaccharide that shares at least some of the rare monosaccharides with RG-II (Matsunaga et al, 2004).…”