Plant Molecular Biology 3:431 444 (1984).
© Martinus N!ihqlf/Dr W. Junk Publishers, Dordrecht. Printed in the Netherlands'.
Molecular biology of C 4 photosynthesis in Zea mays: differential localization of proteins
and mRNAs in the two leaf cell types
Richard Broglie, Gloria Coruzzi, Brian Keith, & Nam-Hai Chua
Laboratory of Plant Molecular Biology, The Rockefeller University, 1230 York Avenue, New York,
NY 10021-6399, U.S.A.
Summary
We have investigated the molecular basis of differential localization of enzyme activities in mesophyll (M)
and bundle-sheath (B) cells of maize leaves. M protoplasts and B strands were prepared by enzymatic
digestions and mechanical treatment of secondary leaves. Soluble and thylakoid membrane proteins from the
two cell types were compared by one- and two-dimensional gel electrophoresis and quantitative rocket
immunoelectrophoresis. In addition, several thylakoid polypeptides were identified by crossed immunoelec-
trophoresis using monospecific antibodies. M and B thylakoids show quantitative and qualitative differences
in their polypeptide compositions. While the M thylakoids contain the normal complement of polypeptides,
the B thylakoids are deficient in ferredoxin-NADP+ reductase, photosystem II reaction center polypeptides,
and the light-harvesting chlorophyll a/b-protein complex. Comparison of the soluble proteins by two-di-
mensional gel electrophoresis revealed marked differences between M and B cells. The major proteins of one
cell type are clearly absent from the other. These differences are paralleled by differences in the in vitro
translation products of poly A + RNA isolated from the two cell types. Immunoprecipitation experiments
showed that mRNA encoding the small subunit of ribulose-l,5-bisphosphate carboxylase (rbcS) is localized
exclusively in B cells, whereas mRNA encoding phosphoenolpyruvate carboxylase is detected only in M cells.
cDNA clones encoding the carboxylase rbcS and the chlorophyll a/b binding protein were used as probes in
Northern blot analysis. M ceils contain no detectable RNA encoding rbcS but have a higher steady state level
of RNA encoding the chlorophyll a/b-binding polypeptide compared to B cells. Taken together, our results
demonstrate that differential gene expression in the two leaf cell types is regulated at the level of translatable
mRNA, and, for at least two proteins, at the level of steady-state RNA.
Introduction
Higher plants may be divided into two groups, C3
and C4, depending on their photosynthetic carbon
assimilation pathway. The primary carbon fixation
reaction in C3 plants is catalyzed by ribulose 1,5-
bisposphate carboxylase/oxygenase (RUBISCO),
while that in Ca plants is catalyzed by phospho-
enolpyruvate carboxylase (PEPC). C4 plants in-
clude such economically important crops such as
maize, sorghum and sugarcane.
A characteristic feature of Ca plants is the differ-
entiation of their photosynthetic cells into two dis-
tinct types, deemed mesophyll (M) and bundle
sheath (B). These cells contain different comple-
ments of photosynthetically important enzymatic
activities and display a precise spatial organization
within the leaf (for a review see Ref. 21). In this
'Krantz' type anatomy, B cells form a layer sur-
rounding the vascular bundle and M cells form a
concentric layer surrounding the B cells. This un-
usual anatomy serves to compartmentalize the bio-
chemical reactions and metabolites characteristic
of C4 photosynthesis. Primary carbon fixation,
mediated by PEPC, occurs in the cytosol of M cells.
In maize, the fixed CO 2 is transported as malate to
B cell chloroplasts, where it is decarboxylated and
the released CO2 refixed via the photosynthetic
carbon reduction cycle. This scheme results in ele-
vated CO2 concentrations at the site of net carbon