Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants.
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.
Matsunaga
Toshiro
T
National Agricultural Research Center for Kyushu Okinawa Region, Nishigoshi, Kumamoto 861-1192, Japan.
Ishii
Tadashi
T
Matsumoto
Sadamu
S
Higuchi
Masanobu
M
Darvill
Alan
A
Albersheim
Peter
P
O'Neill
Malcolm A
MA
D005075:Biological Evolution; D001881:Borates / Q000032:analysis; D001895:Boron / Q000032:analysis; D044002:Bryophyta / Q000235:genetics / Q000378:metabolism; D002240:Carbohydrate Sequence; D002473:Cell Wall / Q000378:metabolism; D029624:Ferns / Q000235:genetics / Q000378:metabolism; D029542:Lycopodiaceae / Q000235:genetics / Q000378:metabolism; D013058:Mass Spectrometry; D008969:Molecular Sequence Data; D010368:Pectins / Q000737:chemistry / Q000378:metabolism*; D010944:Plants / Q000235:genetics* / Q000378:metabolism*; D032503:Selaginellaceae / Q000235:genetics / Q000378:metabolism
D001881:Borates; C042492:rhamnogalacturonan II; D010368:Pectins; D001895:Boron