Patterns of leaf development in C4 plants.

Abstract

REVIEW INTRODUCTIONThe differentiation of cell types in plants depends on the continuous interpretation of positional information. Plant organs are established by patterns of cell division that are often highly variable, yet the final arrangement of cell types within each organ remains the same. A current challenge is to understand the means by which cells of varying clonal history arrive at the same differentiated fate in the development of a plant organ. The ideal system for the study of this developmental control would be an organ with few cell types, with defined patterns of cell origin, and with molecular markers for the differentiation of the individual cell types. The developing C4 leaf is one system that satisfies these requirements. In the leaves of plants capable of C4 carbon fixation, two major photosynthetic cell types--bundle sheath and mesophyll--differentiate as the leaf vascular system is established. The data suggest that bundle sheath (BS) and mesophyll (M) cells must interpret positional information distributed around each vein to express correctly cell-specific genes. Light plays a crucial role in the generation or interpretation of this positional information. This article reviews the available data on the differentiation of these cell types and on the development of the C4 system. C4 Carbon FixationC4 carbon fixation depends on cell-specific gene expression. Neighboring photosynthetic BS and M cells interact in C4 plants to eliminate two inefficiencies of the ribulose bisphosphate carboxylase (RuBPCase)-catalyzed fixation of CO2. In most (C3) plants, 02 competes with CO2 for RuBPCase and the resulting fixed 02 wastes energy via the process of photorespiration. (For reviews on C4 physiology and biochemistry, see Hatch, 1978;Edwards and Huber, 1981;Edwards and Walker, 1983;Furbank and Foyer, 1988.) C4 plants eliminate this 02 inhibition by compartmentalizing the O2-sensitive RuBPCase step away from 02 in internal BS cells and by saturating RuBPCase with high levels of CO2. In a two-cell shuttle, CO2 is first fixed into the C4 acid oxaloacetate by an O2-insensitive carboxylase (phosphoenolpyruvate carboxylase, PEP-1 To whom correspondence should be addressed. Case) in M cells. After conversion to malate or aspartate, the C4 compound is then passed rapidly to neighboring BS cells for release of CO2 and refixation by RuBPCase. A C3 compound is returned to M cells to balance the cycle. C4 carbon metabolism is generally more efficient than the conventional C3 scheme under conditions of high temperature and light intensity. The C4 system is nearly always associated with Kranz leaf anatomy, in which photosynthetic BS and M cells form successive layers around the veins (Hatch and Osmond, 1976). This anatomy is also associated with increased efficiency in water use and is a distinct advantage in arid conditions. The C4 system costs energy, however, and some studies suggest that certain C4 plants can also function as C3 plants when use of the C3 pathway is energetically favorable (Khanna and Sinha, 197...

Differential transcription of plastome-encoded genes in the mesophyll and bundle-sheath chloroplasts of the monocotyledonous NADP-malic enzyme-type C4 plants maize and Sorghum

“…While no bundle-sheath protoplasts were released from maize and Sorghum strands under these conditions -even after digestion for up to 12 h and similar treatment only low yields of bundle-sheath protoplasts were obtained (cf. [27] the procedure rendered the bundle-sheath cells susceptible to breakage by gentle mechanical treatment. After digestion, the bundle-sheath strands were collected in a commercially available tea strainer and then transferred onto a 80 /2m mesh that was submersed in 200 ml of blending medium II.…”

“…As first steps towards an understanding of the mechanisms controlling the C4-specific expression of plastid genes, protein and mRNA levels were investigated using northern and western analysis (reviewed in [27]). For rbcL and the plastome-located photosystem II genes, it has been shown that the differences in the protein levels found in mesophyll and bundle-sheath chloroplasts correlate with differences in the levels of the corresponding transcripts, which implicates that the C4-specific expression of plastid genes is regulated at the level of mRNA abundance [21,29,37,38].…”

Maize F₁ hybrid differs from its maternal parent in the development of chloroplasts in bundle sheath, but not in mesophyll cells: Quantitative analysis of chloroplast ultrastructure and dimensions in different parts of leaf blade at the beginning of its senescence

“…nitrogen assimilation, biosynthesis of lipids) necessitates the preference for a linear photosynthetic electron transport in thylakoid membranes of these cells, and thus for a high amount and photochemical activity of PS2, associated with high granality of MC chloroplasts' thylakoids (Chow et al 2005, Majeran et al 2005. On the other hand, the biosynthesis and the accumulation of starch take place preferentially (but not exclusively) in the BSCs, which are often filled up with starch inclusions (Spilatro and Preiss 1987, Nelson and Langdale 1989, Lunn and Hatch 1995, Majeran et al 2005.…”

“…the bundle sheath cells (BSCs) surrounding the vascular bundles, and the mesophyll cells (MCs), which in turn surround the BSCs. The arrangement of these cells in leaves of NADP-ME plants follows the pattern referred to as the Kranz anatomy (Kranz is the German word for "wreath"), where the two cell layers give the appearance of wreath surrounding each vein (Furbank and Foyer 1988, Nelson and Langdale 1989, Nelson and Dengler 1992, Edwards et al 2001, Leegood 2002, Brown et al 2005. The BSCs and MCs differ in their structural properties; the most conspicuous feature of BSCs being their larger size compared to MCs, their thick cell walls, and the centrifugal or centripetal ---(NAD-malate type) arrangement of chloroplasts (Nelson and Langdale 1989, Dengler et al 1994, Leegood 2002, Brown et al 2005.…”

Expression of a C3 plant Rubisco SSU gene in regenerated C4 Flaveria plants

“…Plants utilizing the C4 pathway of photosynthesis possess a specialized leaf anatomy quite different from the loose arrangement of parenchyma (spongy and palisade mesophyll cells) typical of C3 plants (for review see [24]) C 4 'Kranz' anatomy comprises two major photosynthetically active cell types centrifugally arranged about the vascular bundles. These two cell types cooperate in a multi-step scheme of CO2 fixation, the C4 pathway.…”