Cellular pattern of photosynthetic gene expression in developing maize leaves.

Abstract

Leaf development in C4 plants such as maize involves the differentiation of two photosynthetic cell types [bundle sheath (BS) and mesophyll (M)] to form Kranz-type leaf anatomy. This cellular dimorphism partitions photosynthetic activities so that each enzyme of the C4 pathway accumulates only in the appropriate cell type. We have exploited this property to study BS and M cell interactions in developing maize leaves. Our previous studies showed that C4 proteins appear concurrently with the appearance of Kranz anatomy. To look at earlier events in BS and M cell development we have used three of the corresponding C4 mRNAs as cell-specific markers. We have followed, in situ, the accumulation of malic enzyme (ME), phosphoenolpyruvate carboxylase (PEPCase), and ribulose bisphosphate carboxylase (RuBPCase) mRNAs in developing leaves of both normal and mutant argentia (ar) maize. We have isolated a partial cDNA clone for maize ME to examine ME mRNA expression. We show that throughout the development of light-grown seedlings, all three mRNAs accumulate in a cell-specific fashion in both normal and ar leaves. The pattern of C4 mRNA accumulation longitudinally along the veins, laterally across the leaf, and locally around individual veins reveals the spatial and temporal sequence of BS and M cell development. BS cell-specific mRNAs accumulate around developing veins before Kranz anatomy is evident morphologically. Our analysis of the ar mutant, in which C4 mRNA appearance is delayed relative to the appearance of Kranz anatomy, demonstrates first that BS and M cells develop in clusters across the leaf blade and second that BS cells surrounding any individual vein are activated asynchronously. We discuss our results in relation to models and mechanisms of BS and M cell development.

A Conserved Transcription Factor Mediates Nuclear Control of Organelle Biogenesis in Anciently Diverged Land Plants

“…RNA was isolated, and DNA and RNA gel blots were prepared and hybridized as described by Langdale et al (1988) using gene-specific probes as follows: AtGLK1, 225-bp fragment corresponding to positions 217 to 441 of accession number AY026772; PpGlk1 59 region, 245-bp fragment corresponding to positions 1027 to 1271 of accession number AY741684; PpGlk1 39 region, 292-bp fragment corresponding to positions 1927 to 2218 of accession number AY741684; PpCao, 360-bp…”

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

“…In the C4 monocot maize, both cell position and light influence the bundle sheath cell-specific expression of RuBPCase genes (Sheen andBogarad, 1985, 1986;Langdale et al, 1988aLangdale et al, , 1988bNelson and Langdale, 1989). Recently, we reported that in the C4 dicot amaranth, the developmental stage of the leaf, rather than light, appears to control bundle sheath cell-specific expression of the RuBPCase LSU and SSU genes (Wang et al, 1992).…”

Phosphoenolpyruvate Carboxykinase Is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize1

“…Extracts were boiled for 90 s with equal volumes of solubilization buffer (62.5 mm Tris, 20% [v/v] glycerol, 2.5% [w/v] SDS, and 5% [v/v] 2-mercaptoethanol, pH 6.8). After SDS-PAGE, the proteins were transferred onto a PVDF membrane (Immobilon-P, Millipore) and probed with antisera raised against PEPCK from cucumber , PEPC from Amaranthus edulis, Rubisco from Brassica napus, Ala aminotransferase from barley (Muench and Good, 1994), Asp aminotransferase from Panicum maximum (Numuzawa et al, 1989), and NAD-ME (Murata et al, 1989) and NADP-ME from maize (Langdale et al, 1988). A peroxidaseconjugated secondary antibody was used, and immunoreactive bands were visualized with an enhanced chemiluminescence kit (Amersham).…”