Primary cell wall composition of bryophytes and charophytes.

Major differences in primary cell wall (PCW) components between non-vascular plant taxa are reported. (1) Xyloglucan: driselase digestion yielded isoprimeverose (the diagnostic repeat unit of xyloglucan) from PCW-rich material of Anthoceros (a hornwort), mosses and both leafy and thalloid liverworts, as well as numerous vascular plants, showing xyloglucan to be a PCW component in all land plants tested. In contrast, charophycean green algae (Klebsormidium flaccidium, Coleochaete scutata and Chara corallina), thought to be closely related to land plants, did not contain xyloglucan. They did not yield isoprimeverose; additionally, charophyte material was not digestible with xyloglucan-specific endoglucanase or cellulase to give xyloglucan-derived oligosaccharides. (2) Uronic acids: acid hydrolysis of PCW-rich material from the charophytes, the hornwort, thalloid and leafy liverworts and a basal moss yielded higher concentrations of glucuronic acid than that from the remaining land plants including the less basal mosses and all vascular plants tested. Polysaccharides of the hornwort Anthoceros contained an unusual repeat-unit, glucuronic acid-alpha(1-->3)-galactose, not found in appreciable amounts in any other plants tested. Galacturonic acid was consistently the most abundant PCW uronic acid, but was present in higher concentrations in acid hydrolysates of bryophytes and charophytes than in those of any of the vascular plants. Mannuronic acid was not detected in any of the species surveyed. (3) Mannose: acid hydrolysis of charophyte and bryophyte PCW-rich material also yielded appreciably higher concentrations of mannose than are found in vascular plant PCWs. (4) Mixed-linkage glucan (MLG) was absent from all algae and bryophytes tested; however, upon digestion with licheninase, PCW-rich material from the alga Ulva lactuca and the leafy liverwort Lophocolea bidentata yielded penta- to decasaccharides, indicating the presence of MLG-related polysaccharides. Our results show that major evolutionary events are often associated with changes in PCW composition. In particular, the acquisition of xyloglucan may have been a pre-adaptive advantage that allowed colonization of land.

[1]  J. R. Woodward,et al.  Water-soluble (1→3), (1→4)-β-D-glucans from barley (Hordeum vulgare) endosperm. II. Fine structure , 1983 .

[2]  I. Bremner,et al.  The hemicelluloses of bracken. II. A galactoglucomannan. , 1971, Carbohydrate research.

[3]  K. R. Mattox Classification of the green algae: a concept based on comparative cytology , 1984 .

[4]  N. J. King,et al.  Polysaccharides of the Characeae. III. The carbohydrate content of Chara australis. , 1961, Biochimica et biophysica acta.

[5]  I. Maruyama,et al.  Isolation and Identification of 2-O-Methyl-l-rhamnose and 3-O-Methyl-l-rhamnose as Constituents of an Acidic Polysaccharide of Chlorella vulgaris , 1997 .

[6]  J. Dumville,et al.  Uronic acid-containing oligosaccharins : Their biosynthesis, degradation and signalling roles in non-diseased plant tissues , 2000 .

[7]  S. Yamamoto,et al.  Blood-group active proteoglycan containing 3-O-methylrhamnose (acofriose) from young plants of Osmunda japonica. , 1988, Carbohydrate research.

[8]  Park S. Nobel,et al.  Biophysical plant physiology and ecology , 1983 .

[9]  N. R. Williams,et al.  DEOXY AND BRANCHED-CHAIN SUGARS , 1981 .

[10]  I. Bremner,et al.  The hemicelluloses of bracken , 1966 .

[11]  J. Palmer,et al.  The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants , 1990, Nature.

[12]  J. Pickett-Heaps Cell Division in Eucaryotic Algae , 1976 .

[13]  P. Albersheim,et al.  An unambiguous nomenclature for xyloglucan‐derived oligosaccharides , 1993 .

[14]  K. Waldron,et al.  Physiology and Biochemistry of Plant Cell Walls , 1990, Topics in Plant Physiology.

[15]  N. K. Matheson,et al.  11 - Mannose-based Polysaccharides , 1990 .

[16]  G. Cassab,et al.  PLANT CELL WALL PROTEINS. , 1998, Annual review of plant physiology and plant molecular biology.

[17]  V. Das,et al.  Non-Volatile Organic Acids in Some Liverworts , 1963, Nature.

[18]  Z. Popper,et al.  3-O-methyl-D-galactose residues in lycophyte primary cell walls. , 2001, Phytochemistry.

[19]  Peter R. Crane,et al.  The origin and early evolution of plants on land , 1997, Nature.

[20]  W. Barthlott,et al.  Ultrastructure and chemistry of the cell wall of the moss Rhacocarpus purpurascens (Rhacocarpaceae): a puzzling architecture among plants , 1998, Planta.

[21]  S. Churchill,et al.  A cladistic approach to the phylogeny of the “Bryophytes” , 1984 .

[22]  Derekt . A. Lamport,et al.  Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. , 1994, The Plant journal : for cell and molecular biology.

[23]  P. Albersheim,et al.  Structure of Plant Cell Walls : XIX. Isolation and Characterization of Wall Polysaccharides from Suspension-Cultured Douglas Fir Cells. , 1987, Plant physiology.

[24]  L. Graham Origin of land plants , 1993 .

[25]  R. Cleland,et al.  Differences in the occurrence and distribution of hydroxyproline-proteins among the algae. , 1968, American journal of botany.

[26]  B. Mishler,et al.  TRANSITION TO A LAND FLORA: PHYLOGENETIC RELATIONSHIPS OF THE GREEN ALGAE AND BRYOPHYTES , 1985, Cladistics : the international journal of the Willi Hennig Society.

[27]  D. Garbary,et al.  Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[28]  G. Stebbins COMPARATIVE ASPECTS OF PLANT MORPHOGENESIS: A CELLULAR, MOLECULAR, AND EVOLUTIONARY APPROACH , 1992 .

[29]  Morrison Jc,et al.  Cell wall synthesis during growth and maturation of Nitella internodal cells. , 1993 .

[30]  Stephen C. Fry,et al.  The Growing Plant Cell Wall: Chemical and Metabolic Analysis , 2001 .

[31]  I. Capesius,et al.  New Aspects of Bryophyte Taxonomy Provided by a Molecular Approach , 1996 .

[32]  N. Carpita,et al.  Plant Cell Walls , 2001, Springer Netherlands.

[33]  C. Delwiche,et al.  Phylogenetic Relationships of the "Green Algae" and "Bryophytes" , 1994 .

[34]  C. Morvan,et al.  Structural features of water-soluble pectins from mung bean hypocotyls , 1994 .

[35]  P Albersheim,et al.  Structure of Plant Cell Walls: XI. GLUCURONOARABINOXYLAN, A SECOND HEMICELLULOSE IN THE PRIMARY CELL WALLS OF SUSPENSION-CULTURED SYCAMORE CELLS. , 1980, Plant physiology.

[36]  Jeffrey B. Harborne,et al.  Methods in plant biochemistry , 1989 .

[37]  Paul G. Wolf,et al.  Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants , 2001, Nature.

[38]  S. Kauppinen,et al.  A xyloglucan-specific endo-beta-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. , 1999, Glycobiology.

[39]  N. Carpita,et al.  Synthesis of (1-->3), (1-->4)-beta-D-glucan in the Golgi apparatus of maize coleoptiles. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. C. Scheirer Differentiation of Bryophyte Conducting Tissues: Structure and Histochemistry , 1980 .

[41]  L. Greve,et al.  Cell wall synthesis during growth and maturation of Nitella internodal cells , 2004, Planta.

[42]  C. Sensen,et al.  The origin of land plants: Phylogenetic relationships among charophytes, bryophytes, and vascular plants inferred from complete small-subunit ribosomal RNA gene sequences , 1995, Journal of Molecular Evolution.

[43]  C. Stace Plant taxonomy and biosystematics , 1981 .

[44]  Philip J. Harris,et al.  Monosaccharide compositions of unlignified cell walls of monocotyledons in relation to the occurrence of wall-bound ferulic acid , 1997 .

[45]  T. Hedderson,et al.  Phylogenetic relationships of bryophytes inferred from nuclear-encoded rRNA gene sequences , 1996, Plant Systematics and Evolution.

[46]  D.M.W. Anderson,et al.  The presence of 3-O-methylrhamnose in araucaria resinous exudates , 1969 .