Annu Rev Plant Physiol Plant Mol Biol 1996 47 445 476 Downloaded from arjournals annualreviews org by University of Georgia on 04 26 06 For personal use only Annu Rev Plant Physiol Plant Mol Biol 1996 47 445 76 Copyright 1996 by Annual Reviews Inc All rights reserved STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES Nicholas C Carpita Department of Botany and Plant Pathology Purdue University West Lafayette Indiana 47907 KEY WORDS cereals grasses cell wall polysaccharides cell wall biosynthesis cell wall architecture ABSTRACT The chemical structures of the primary cell walls of the grasses and their progenitors differ from those of all other flowering plant species They vary in the complex glycans that interlace and cross link the cellulose microfibrils to form a strong framework in the nature of the gel matrix surrounding this framework and in the types of aromatic substances and structural proteins that covalently cross link the primary and secondary walls and lock cells into shape This review focuses on the chemistry of the unique polysaccharides aromatic substances and proteins of the grasses and how these structural elements are synthesized and assembled into dynamic and functional cell walls Despite wide differences in wall composition the developmental physiology of grasses is similar to that of all flowering plants Grass cells respond similarly to environmental cues and growth regulators exhibit the same alterations in physical properties of the wall to allow cell growth and possess similar patterns of wall biogenesis during the development of specific cell and tissue types Possible unifying mechanisms of growth are suggested to explain how grasses perform the same wall functions as other plants but with different constituents and architecture CONTENTS INTRODUCTION THE STRUCTURAL ELEMENTS OF THE PRIMARY WALLS OF THE POACEAE Cellulose Glucuronoarabinoxylans The 1 3 1 4 D glucans 1040 2519 96 0601 0445 08 00 446 447 447 447 448 445 446 CARPITA Annu Rev Plant Physiol Plant Mol Biol 1996 47 445 476 Downloaded from arjournals annualreviews org by University of Georgia on 04 26 06 For personal use only Xyloglucan Other Glycans Pectic Substances Aromatic Substances Structural Proteins Other Cell Wall Substances CELL WALL COMPOSITION AS A TAXONOMIC CHARACTER IN THE MONOCOTYLEDONAE 450 450 450 451 453 454 454 ARCHITECTURE 458 STRUCTURAL DYNAMICS DURING CELL ELONGATION 462 CELL WALL BIOGENESIS IN GRASSES 465 Biosynthesis of 1 3 1 4 D Glucan 466 Biosynthesis of Other Cell Wall Polysaccharides 467 GENETIC MODELS OF CELL WALL DEVELOPMENT IN THE GRASSES 467 INTRODUCTION In the early 1900s Walter Norman Haworth and Edmund Langley Hirst founding fathers of modern carbohydrate chemistry began studies of the pentose constituents of cell walls of plants Armed with only rudimentary analytical techniques they and their colleagues defined the cell walls of esparto grass as composed largely of 1 4 D xylans 58 By 1970 gas chromatography mass spectrometry GC MS was employed routinely for unequivocal determination of linkage structure of complex cell wall polysaccharides Techniques such as 1H and 13C nuclear magnetic resonance NMR spectroscopy provided anomeric configurations linkage structures and some three dimensional configurations Sequence dependent endoglycanases were used to cleave polysaccharides into oligosaccharides that could be completely sequenced From characteristic repeating unit structures the sequence and conformation of very large polymers were deduced 20 By such analyses the major polysaccharides of the walls of a wide range of flowering plants were defined and the first models of how cell walls are put together emerged In subsequent years the dynamic interactions of individual components were reflected in more current models of the architecture of the primary cell wall of flowering plants a strong framework of cellulose microfibrils intertwined with xyloglucans that is embedded in a gel of uronic acid rich pectins and cross linked with hydroxyproline rich glycoproteins 20 101 When the first conceptual models were proposed about twenty years ago the differences in wall compositions between monocots and dicots were just beginning to be catalogued 33 Perhaps because of the socioeconomic importance of the cereals the vast majority of the monocots studied were grasses Whistler 164 described grasses as rich sources of xylan and Aspinall 1 in a review of plant cross linking glycans noted the enrichment of xylans and mixed linked glucans in grasses Wilkie 165 offered the first comprehensive survey of the cross linking glycans of grasses More recent Annu Rev Plant Physiol Plant Mol Biol 1996 47 445 476 Downloaded from arjournals annualreviews org by University of Georgia on 04 26 06 For personal use only CELL WALLS OF GRASSES 447 studies of the carbohydrate and aromatic components of cell walls from a broad spectrum of monocots have revealed that the Poales family Poaceae formerly the order Graminales family Gramineae their progenitors and related taxonomic orders have primary cell walls completely different from those of other monocots 3 20 68 Dahlgren et al 32 proposed phyletical relationships between some two dozen orders of the Monocotyledonae on the basis of several anatomical features and chemical constituents One of these features the presence or absence of ferulic acid in the primary walls is a major distinguishing feature of the Poales and related orders 56 Nonlignified cells of grasses are enriched in aromatic substances and polymeric forms constitute a second architectural element A third type of architectural element is structural protein The primary walls of the Poales contain substantially less protein than other species but several classes of proteins are found in elevated amounts in specific cell types during differentiation Recent reviews 83 147 note that the grass wall proteins bear reasonable homology to those representing major classes of structural proteins of nongramineous species In an earlier review 20 structural models for two types of primary walls were provided the Type I wall composed of a cellulose xyloglucan framework embedded in a pectin gel and the Type II wall the special wall of the Poales This review focuses on the Type II wall of the Poales its composition architecture biogenesis and dynamics during growth THE STRUCTURAL ELEMENTS OF THE PRIMARY WALLS OF THE POACEAE Cellulose Cellulose microfibrils in all flowering plants are composed of about