Evolution and development of cell walls in cereal grains

Abstract

The composition of cell walls in cereal grains and other grass species differs markedly from walls in seeds of other plants. In the maternal tissues that surround the embryo and endosperm of the grain, walls contain higher levels of cellulose and in many cases are heavily lignified. This may be contrasted with walls of the endosperm, where the amount of cellulose is relatively low, and the walls are generally not lignified. The low cellulose and lignin contents are possible because the walls of the endosperm perform no load-bearing function in the mature grain and indeed the low levels of these relatively intractable wall components are necessary because they allow rapid degradation of the walls following germination of the grain. The major non-cellulosic components of endosperm walls are usually heteroxylans and (1,3;1,4)-β-glucans, with lower levels of xyloglucans, glucomannans, and pectic polysaccharides. Pectic polysaccharides and xyloglucans are the major non-cellulosic wall constituents in most dicot species, in which (1,3;1,4)-β-glucans are usually absent and heteroxylans are found at relatively low levels. Thus, the "core" non-cellulosic wall polysaccharides in grain of the cereals and other grasses are the heteroxylans and, more specifically, arabinoxylans. The (1,3;1,4)-β-glucans appear in the endosperm of some grass species but are essentially absent from others; they may constitute from zero to more than 45% of the cell walls of the endosperm, depending on the species. It is clear that in some cases these (1,3;1,4)-β-glucans function as a major store of metabolizable glucose in the grain. Cereal grains and their constituent cell wall polysaccharides are centrally important as a source of dietary fiber in human societies and breeders have started to select for high levels of non-cellulosic wall polysaccharides in grain. To meet end-user requirements, it is important that we understand cell wall biology in the grain both during development and following germination.

Keywords: (1,3;1,4)-β-glucan; arabinoxylans; biosynthesis; cellulose; evolution; non-cellulosic polysaccharides.

FIGURE 1

(A) Examples of different grain morphologies. (B) Hard and soft endosperm proportions vary in maize kernels. Reproduced with permission from Hands and Drea (2012) and http://www.deductiveseasoning.com/2014/03/planting-and-growing-corn-for-nutrition.html. In panel (A), em, embryo; en, endosperm; ma, modified aleurone; cav, cavity; va, vasculature; ne, nucellar epidermis; np, nucellar projection; BETL, basal endosperm transfer layer.

FIGURE 2

Changes in cell wall composition during the development of barley coleoptiles. Compositions were deduced from data obtained by alditol acetate, methylation and acetic–nitric acid analyses. Changes in cellulose (filled square), arabinoxylan (AX, open square), pectic polysaccharides (pectin, open circle), xyloglucan (XylG, triangle), and (1,3;1,4)-β-glucan (MLG, filled circle) are shown. Reproduced with permission from Gibeaut et al. (2005).

FIGURE 3

Different stages of endosperm development in barley. Light micrographs of sections through barley grains showing stages of endosperm development from 3 to 8 DAP. (A) 3 DAP: a thin layer of syncytial cytoplasm surrounds a large central vacuole. (B) Details of the syncytium in (A). Arrows indicate the position of nuclei along the perimeter of the central cell, all enclosed within discrete layers of maternal tissue. (C) 5 DAP: cellularization occurs centripetally with repeated cycles of anticlinal wall formation, mitosis and periclinal wall formation. (D) 4 DAP: shows the wavy appearance of anticlinal walls (arrow) and a periclinal wall (arrowhead) separating two recently divided daughter nuclei. (E) 8 DAP: the endosperm was fully cellularized and starch granules (arrows) had accumulated within each cell. cv, central vacuole; i, integuments; n, nucellus; p, pericarp. Scale bars = 300 μm (A,C), 50 μm (B,E), 20 μm (D). Reproduced with permission from Wilson et al. (2006).

FIGURE 4

Different types of transfer cells (TC) in cereals and other seeds. These images of TC of developing seeds illustrate various ingrowth wall morphologies. (A) Epidermal transfer cells (ETC) of a Vicia faba cotyledon with an extensive reticulate ingrowth wall labyrinth including clumps of ingrowth material (arrow) and smaller wall ingrowths in the subepidermal cells (SEC; arrowhead). (B) Basal endosperm TC of Zea mays exhibiting flange wall ingrowth morphology; arrowheads indicate small lateral protrusions from the linear ribs (modified after Talbot et al., 2002). (C) Thin-walled parenchyma TC located at the inner surface of the inner seed coat of Gossypium hirsutum with wall ingrowth flanges (darts) extending the length of each cell on which are deposited groups of reticulate wall ingrowths (arrows; modified after Pugh et al., 2010). (D–F) Transmission electron microscope images of portions of transverse sections of TC: (D) the outer periclinal wall of an adaxial epidermal cell of a V. faba cotyledon induced to trans-differentiate to a transfer cell morphology displaying primary wall (PW) and uniform walls (UW). (E) Small papillate ingrowths (darts) of a seed coat transfer cell of V. faba exhibiting reticulate architecture. (F) Antler-shaped reticulate wall ingrowths (darts) of a nucellar projection transfer cell of a developing Triticum turgidum var. durum seed (modified after Wang et al., 1994). (G) Field emission scanning electron microscope image of the cytoplasmic face of the reticulate ingrowth wall labyrinth of an abaxial epidermal transfer cell of a V. faba cotyledon following removal of the cytoplasm and dry cleaving (for method see Talbot et al. (2001), image modified after Talbot et al. (2001)) where the darts indicate ingrowth papillae on the most recently deposited wall layer. Single scale bar for (A,B) = 2.5 μm; for (C) = 5 μm; for (D,E) = 1 μm; for (F) = 0.25 μm; for (G) = 0.5 μm. Figure legend and images reproduced with permission from Andriunas et al. (2013).

FIGURE 5

Diagrammatical representations of the major non-cellulosic wall polysaccharides from cereal grains. The (1,3;1,4)-β-glucan (left) has relatively extended regions of adjacent (1,4)-β-glucosyl residues (blue) with irregularly spaced, single (1,3)-β-glucosyl residues. The latter residues form molecular “kinks” in the polysaccharide chain and limit intermolecular alignment and microfibril formation. In the heteroxylan (right), intermolecular alignment of the xylan backbone (stars) and microfibril formation is limited by steric hindrance afforded by the substituents (blue, pink, etc.). Reproduced with permission from Burton et al. (2010).

FIGURE 6

Thick endosperm cell walls in Brachypodium distachyon grain. Reproduced with permission from Trafford et al. (2013).

FIGURE 7

Thin section of a young barley leaf probed with the BG1 monoclonal antibody. The high concentration of (1,3;1,4)-β-glucans can be seen around the vasculature and the polysaccharide appears to be associated with secondary cell walls of the vasculature and other cells. Reproduced with permission from Burton et al. (2011).