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Transcriptional control of aspartate kinase expression during darkness and sugar depletion in Arabidopsis: involvement of bZIP transcription factors

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Abstract

Initial steps of aspartate-derived biosynthesis pathway (Asp pathway) producing Lys, Thr, Met and Ile are catalyzed by bifunctional (AK/HSD) and monofunctional (AK-lys) aspartate kinase (AK) enzymes. Here, we show that transcription of all AK genes is negatively regulated under darkness and low sugar conditions. By using yeast one-hybrid assays and complementary chromatin immunoprecipitation analyses in Arabidopsis cells, the bZIP transcription factors ABI5 and DPBF4 were identified, capable of interacting with the G-box-containing enhancer of AK/HSD1 promoter. Elevated transcript levels of DPBF4 and ABI5 under darkness and low sugar conditions coincide with the repression of AK gene expression. Overexpression of ABI5, but not DPBF4, further increases this AK transcription suppression. Concomitantly, it also increases the expression of asparagines synthetase 1 (ASN1) that shifts aspartate utilization towards asparagine formation. However, in abi5 or dpbf4 mutant and abi5, dpbf4 double mutant the repression of AK expression is maintained, indicating a functional redundancy with other bZIP-TFs. A dominant-negative version of DPBF4 fused to the SRDX repressor domain of SUPERMAN could counteract the repression and stimulate AK expression under low sugar and darkness in planta. This effect was verified by showing that DPBF4-SRDX fails to recognize the AK/HSD1 enhancer sequence in yeast one-hybrid assays, but increases heterodimmer formation with DPBF4 and ABI5, as estimated by yeast two-hybrid assays. Hence it is likely that heterodimerization with DPBF4-SRDX inhibits the binding of redundantly functioning bZIP-TFs to the promoters of AK genes and thereby releases the repressing effect. These data highlight a novel transcription control of the chloroplast aspartate pathway that operates under energy limiting conditions.

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Abbreviations

AK/HSD1:

Bifunctional aspartate kinase-homoserine dehydrogenase

AK-lys1(2, 3):

Monofunctional aspartate kinases

bZIP-TF:

Basic DNA binding domain—leucine zipper—transcription factor

ChIP:

Chromatin immunoprecipitation

DPBF, DC3:

Promoter-binding factor

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Acknowledgments

We are grateful to Prof. R. Finkelstein (University of California at Santa Barbara, CA, USA) for providing the ABI5-overexpressing and abi5-1 mutants, and Prof. NH Chua (Rockefeller University, New York, USA) for the pER8 vector. We thank Sabine Schaefer and Ingrid Reinsch for technical help, Dr. Haviva Eilenberg and Dr. Kenneth Berendzen for helpful discussions. This work was supported by Minna and James Heineman Foundation (G.G. and C.K.), European Union FP5 (OLRT-2001-00841) (C.K. and A.Z.), Deutsche Forschungsgemenischaft SFB635 and AFGN (KO 1438/12-1) (C.K.), DFG German-Israeli-Palestinian Trilateral grant (KO 1438/13-1) (CK and AZ.), and European Union COST FA0605 grant (G.G, C.K and A.Z.).

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Authors and Affiliations

  1. Department of Plant Sciences, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel

    Shai Ufaz, Yulia Soloveichik, Yelena Golan & Aviah Zilberstein

  2. Max-Planck Institut für Züchtungsforschung, Carl-von-Linne-Weg 10, 50829, Köln, Germany

    Vijaya Shukla, Frank Breuer, Zsuzsa Koncz & Csaba Koncz

  3. KWS SAAT AG, 37555, Einbeck, Germany

    Frank Breuer

  4. Department of Plant Sciences, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Gad Galili

  5. Institute of Plant Biology, Biological Research Center of Hungarian Academy of Sciences, 6724, Szeged, Hungary

    Csaba Koncz

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  1. Shai Ufaz
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Correspondence to Aviah Zilberstein.

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S. Ufaz, V. Shukla, C. Koncz and A. Zilberstein have equally contributed to this work.

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Ufaz, S., Shukla, V., Soloveichik, Y. et al. Transcriptional control of aspartate kinase expression during darkness and sugar depletion in Arabidopsis: involvement of bZIP transcription factors. Planta 233, 1025–1040 (2011). https://doi.org/10.1007/s00425-011-1360-9

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