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J. Biol. Chem., Vol. 281, Issue 35, 25485-25491, September 1, 2006

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Untranslated Regions of FbRbcS1 mRNA Mediate Bundle Sheath Cell-specific Gene Expression in Leaves of a C₄ Plant^*

From the Department of Biological Sciences, State University of New York, Buffalo, New York 14260

C₄ photosynthesis typically requires two specialized leaf cell types, bundle sheath (bs) and mesophyll (mp), which provide the foundation for this highly efficient carbon assimilation pathway. In leaves of Flaveria bidentis, a dicotyledonous C₄ plant, ribulose 1,5-bisphosphate carboxylase (rubisco) accumulates only in bs cells surrounding the vascular centers and not in mp cells. This is in contrast to the more common C₃ plants, which accumulate rubisco in all photosynthetic cells. Many previous studies have focused on transcriptional control of C₄ cell type-specificity; however, post-transcriptional regulation has also been implicated in the bs-specific expression of genes encoding the rubisco subunits. In this current study, a biolistic leaf transformation assay has provided direct evidence that the 5'- and 3'-untranslated regions (UTRs) of F. bidentis FbRbcS1 mRNA (from a nuclear gene encoding the rubisco small subunit), in themselves, confer strong bs cell-specific expression to gfpA reporter gene transcripts when transcribed from a constitutive CaMV promoter. In transformed leaf regions, strong bs cell-specific GFP expression was accompanied by corresponding bs cell-specific accumulation of the constitutively transcribed FbRbcS1 5'-UTR-gfpA-3'-UTR mRNAs. Control constructs lacking any RbcS mRNA sequences were expressed in all leaf cell types. These findings demonstrate that characteristic cell type-specific FbRbcS1 expression patterns in C₄ leaves can be established entirely by sequences contained within the transcribed UTRs of FbRbcS1 mRNAs. We conclude that selective transcript stabilization (in bs cells) or degradation (in mp cells) plays a key role in determining bs cell-specific localization of the rubisco enzyme.

Received for publication, May 1, 2006 , and in revised form, June 14, 2006.

^* This work was supported by Grants 2001-01825 from United States Department of Agriculture/National Research Initiative and MCB 0110411 from the National Science Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental primer material and supplemental Figs. S1 and S2.

¹ Current address: USDA ARS Cereal Crops Research Unit, Barley and Malt Laboratory, 501 Walnut St., Madison, WI 53726.

² To whom correspondence should be addressed: Dept. of Biological Sciences, State University of New York, Buffalo, NY 14260. Tel.: 716-645-2363 (ext. 145); Fax: 716-645-3369; E-mail: camjob{at}buffalo.edu.

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