Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses.

A major part of the daily caloric intake of human societies around the world is derived from a diverse range of foods prepared from members of the grass family, including wheat (Triticum aestivum), rice (Oryza sativa), sorghum (Sorghum bicolor), the millets (Panicum miliaceum and Pennisetum americanum), barley (Hordeum vulgare), and sugar cane (Saccharum officinarum). Grasses cover perhaps 20% or more of the earth’s land surface (Gaut, 2002), and many of these are used as forage and fodder for the production of sheep, cattle, and other domesticated livestock. Maize (Zea mays) is also used widely in animal feed diets, while sorghum, switchgrass (Panicum virgatum), and several other perennial grasses are attracting considerable attention as future biomass energy crops (McLaren, 2005). The grasses are noteworthy for the unusual composition of their cell walls, because walls of grasses have less pectin and xyloglucan, but more heteroxylan, than walls from other higher plants. Most significantly, walls of the grasses contain as major constituents the (1,3;1,4)-b-D-glucans, which are not widely distributed outside the Poaceae. The compositions of walls from selected barley organs are shown in Table I. In many cases, constituents of cell walls in the grasses are closely linked with their widespread adoption, utility, and future potential in agricultural practice and energy production. The noncellulosic polysaccharides of walls in grasses are important components of dietary fiber, which is highly beneficial for lowering the risk of serious human health conditions, including colorectal cancer, high serum cholesterol and cardiovascular disease, obesity, and non-insulin-dependent diabetes (Braaten et al., 1994; Brennan and Cleary, 2005). Conversely, the noncellulosic wall polysaccharides from walls of cereals and grasses have antinutritive effects in monogastric animals such as pigs and poultry (Brennan and Cleary, 2005) and are often considered to be undesirable components of raw materials in the malting and brewing industries (Kuntz and Bamforth, 2007). Although there have been exciting new discoveries in the synthesis of cellulose, pectic polysaccharides, mannans, and xyloglucans in recent years, these discoveries have been made predominantly in dicotyledonous plants (Ye et al., 2006; Mohnen, 2008; Zabotina et al., 2008) and will not be covered here. This update, therefore, will be restricted to recent advances in our understanding of the biosynthesis of the characteristic and major wall polysaccharides of the grasses, namely the heteroxylans and (1,3;1,4)-b-D-glucans. So, why might we argue that we have come upon revolutionary times in our understanding of cell wall biosynthesis in the grasses?What new information has come to light in recent years? Progress in defining the genes and biological mechanisms underlying the synthesis of the major polysaccharides of walls in the grasses had remained painfully slow throughout the biochemical and molecular biological eras, mainly because the enzymes that catalyze the biosynthetic reactions are membrane proteins that usually lose activity quickly after cell disruption, before purification of the enzymes can be effected. Without even partially purified enzyme preparations, we were unable to obtain amino acid sequence information and hence could not identify the corresponding genes. However, emerging technologies of forward and reverse genetics and functional genomics have provided new tools to tackle these difficult problems and have yielded spectacular results. Thus, comparative genomics and forward genetics have been used to identify candidate genes that encode polysaccharide synthases involved in (1,3;1,4)-b-D-glucan biosynthesis in the grasses, while powerful bioinformatic techniques are providing important clues and candidates for the enzymes that mediate in the biosynthesis of the other key wall polysaccharide of the grasses, namely the heteroxylans. Data generated in these studies have raised ancillary but fundamental questions about the subcellular location of wall polysaccharide synthesis in the grasses. Is the Golgi apparatus the only site for the complete synthesis of matrix phase polysaccharides of the wall, including the (1,3;1,4)-b-D-glucans and the heteroxylans, or are there other possibilities? Functional genomics analyses have also pointed to previously unsuspected roles for hydrolytic enzymes and transglycosylases in wall polysaccharide synthe1 This work was supported by the Australian Research Council, the Grains Research and Development Corporation, and the CSIRO Flagship Collaboration Fund. * E-mail [email protected]. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Geoffrey B. Fincher ([email protected]). www.plantphysiol.org/cgi/doi/10.1104/pp.108.130096