Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves.

A selection of C4 species was surveyed to determine the relationship between their content of C4 acid decarboxylating enzymes, the activities of several other enzymes implicated in the C4 pathway, and their anatomical and ultrastructural features. The species examined clearly fell into three groups according to whether they contained high levels of either NADP malic enzyme (EC 1.1.1.40), phosphoenolpyruvate carboxykinase (EC 4.1.1.49) or NAD malic enzyme (EC 1.1 .1.39). The occurrence of high NADP malic enzyme activity was always associated with higher NADP malate dehydrogenase activity, while those species distinguished by high activities of either of the other two decarboxylases invariably contained high aspartate aminotransferase and alanine amino- transferase activities. Each of these decarboxylating enzymes was located in bundle sheath cells. NAD malic enzyme, but not phosphoenolpyruvate carboxykinase, was associated with mitochondria. Light and electron micrographs revealed differences between these groups with respect to the intracellular location of chloroplasts and mitochondria in bundle sheath cells, and the content and ultrastructure of mitochondria. The trend was for species with high NAD malic enzyme to contain the most mitochondria in the bundle sheath cells with apparently the most extensively developed cristae membrane systems. However, mitochondrial respiratory enzyme activities were similar for the three groups of species. The basic similarities and differences between the three groups of C4 plants distinguished by their differing C4 acid decarboxylating systems are discussed, and schemes for the probable photosynthetic reactions in bundle sheath cells are presented. A nomenclature to distinguish between these groups is proposed.

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bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves

Development ◽

10.1242/dev.120.3.673 ◽

1994 ◽

Vol 120 (3) ◽

pp. 673-681 ◽

Cited By ~ 1

Author(s):

J. A. Langdale ◽

C. A. Kidner

Keyword(s):

Gene Action ◽

Morphological Differentiation ◽

Cell Types ◽

Bundle Sheath ◽

Sheath Cell ◽

Mesophyll Cells ◽

Bundle Sheath Cell ◽

Bundle Sheath Cells ◽

Maize Leaves ◽

Sheath Cells

Post-primordial differentiation events in developing maize leaves produce two photosynthetic cell types (bundle sheath and mesophyll) that are morphologically and biochemically distinct. We have isolated a mutation that disrupts the differentiation of one of these cell types in light-grown leaves. bundle sheath defective 1-mutable 1 (bsd1-m1) is an unstable allele that was induced by transposon mutagenesis. In the bundle sheath cells of bsd1-m1 leaves, chloroplasts differentiate aberrantly and C4 photosynthetic enzymes are absent. The development of mesophyll cells is unaffected. In dark-grown bsd1-m1 seedlings, morphological differentiation of etioplasts is only disrupted in bundle sheath cells but photosynthetic enzyme accumulation patterns are altered in both cell types. These data suggest that, during normal development, the Bsd1 gene directs the morphological differentiation of chloroplasts in a light-independent and bundle sheath cell-specific fashion. In contrast, Bsd1 gene action on photosynthetic gene expression patterns is cell-type independent in the dark (C3 state) but bundle sheath cell-specific in the light (C4 state). Current models hypothesize that C4 photosynthetic differentiation is achieved through a light-induced interaction between bundle sheath and mesophyll cells (J. A. Langdale and T. Nelson (1991) Trends in Genetics 7, 191–196). Based on the data shown in this paper, we propose that induction of the C4 state restricts Bsd1 gene action to bundle sheath cells.

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