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Research ArticleResearch Article
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An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells

Ben P. Williams, Steven J. Burgess, Ivan Reyna-Llorens, Jana Knerova, Sylvain Aubry, Susan Stanley, Julian M. Hibberd
Ben P. Williams
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Steven J. Burgess
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Ivan Reyna-Llorens
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Jana Knerova
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Sylvain Aubry
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Susan Stanley
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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Julian M. Hibberd
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
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  • For correspondence: jmh65@cam.ac.uk

Published February 2016. DOI: https://doi.org/10.1105/tpc.15.00570

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  • © 2016 American Society of Plant Biologists. All rights reserved.

Abstract

C4 photosynthesis is a complex phenotype that allows more efficient carbon capture than the ancestral C3 pathway. In leaves of C4 species, hundreds of transcripts increase in abundance compared with C3 relatives and become restricted to mesophyll (M) or bundle sheath (BS) cells. However, no mechanism has been reported that regulates the compartmentation of multiple enzymes in M or BS cells. We examined mechanisms regulating CARBONIC ANHYDRASE4 (CA4) in C4 Gynandropsis gynandra. Increased abundance is directed by both the promoter region and introns of the G. gynandra gene. A nine-nucleotide motif located in the 5′ untranslated region (UTR) is required for preferential accumulation of GUS in M cells. This element is present and functional in three additional 5′ UTRs and six 3′ UTRs where it determines accumulation of two isoforms of CA and pyruvate,orthophosphate dikinase in M cells. Although the GgCA4 5′ UTR is sufficient to direct GUS accumulation in M cells, transcripts encoding GUS are abundant in both M and BS. Mutating the GgCA4 5′ UTR abolishes enrichment of protein in M cells without affecting transcript abundance. The work identifies a mechanism that directs cell-preferential accumulation of multiple enzymes required for C4 photosynthesis.

  • Glossary

    M
    mesophyll
    BS
    bundle sheath
    CA
    carbonic anhydrase
    UTR
    untranslated region
    MUG
    4-methylumbulliferone-glucuronide
    miRNA
    microRNA
    MS
    Murashige and Skoog
    MU
    4-methylumbulliferone
    • Received July 6, 2015.
    • Revised December 18, 2015.
    • Accepted January 13, 2016.
    • Published January 15, 2016.

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    An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells
    Ben P. Williams, Steven J. Burgess, Ivan Reyna-Llorens, Jana Knerova, Sylvain Aubry, Susan Stanley, Julian M. Hibberd
    The Plant Cell Feb 2016, 28 (2) 454-465; DOI: 10.1105/tpc.15.00570

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    An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells
    Ben P. Williams, Steven J. Burgess, Ivan Reyna-Llorens, Jana Knerova, Sylvain Aubry, Susan Stanley, Julian M. Hibberd
    The Plant Cell Feb 2016, 28 (2) 454-465; DOI: 10.1105/tpc.15.00570
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