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Sucrose synthase and RuBisCo expression is similarly regulated by the nitrogen source in the nitrogen-fixing cyanobacterium Anabaena sp.

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Abstract

In higher plants and cyanobacteria, sucrose (Suc) metabolism is carried out by a similar set of enzymes. The function and regulation of Suc metabolism in cyanobacteria has begun to be elucidated. In strains of Anabaena sp., filamentous nitrogen-fixing cyanobacteria, Suc synthase (SuS, EC 2.4.1.13) controls Suc cell level through the cleavage of the disaccharide. The present work shows that there are two sus genes in Anabaena (Nostoc) sp. that are co-regulated regarding the nitrogen source; however, only susA accounts for the extractable SuS activity and for the control of the Suc level. Primer extension analysis has uncovered the sequence of the Anabaena susA and susB ammonium-activated putative promoters, which share a high sequence similarity with that of rbcLS encoding ribulose bisphosphate carboxylase/oxygenase (EC 4.1.1.39) and other ammonium up-regulated genes. Moreover, susA and rbcLS expression is developmentally co-localized to the vegetative cells of the nitrogen-fixing cyanobacterial filaments. Our results strongly suggest the existence of a regulatory network that would coordinate the expression of key genes for Suc and nitrogen metabolism, carbon fixation, and development in Anabaena sp.

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Abbreviations

Chl:

Chlorophyll

gfp :

Green fluorescent protein gene

rbcLS :

Ribulose bisphosphate carboxylase/oxygenase gene

RuBisCO:

Ribulose bisphosphate carboxylase/oxygenase

sus :

Sucrose synthase gene

Suc:

Sucrose

SusB:

Gene product of susB

SuS:

Sucrose synthase

tsp:

Transcription start point

References

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409

    Article  PubMed  CAS  Google Scholar 

  • Cai Y, Wolk CP (1990) Use of a conditionally lethal gene in Anabaena sp.strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172:3138–3145

    PubMed  CAS  Google Scholar 

  • Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33–38

    Article  PubMed  CAS  Google Scholar 

  • Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253

    Article  PubMed  CAS  Google Scholar 

  • Cumino A, Curatti L, Giarrocco L, Salerno GL (2002) Sucrose metabolism: Anabaena sucrose-phosphate synthase and sucrose-phosphate phosphatase define minimal functional domains shuffled during evolution. FEBS Lett 517:19–23

    Article  PubMed  CAS  Google Scholar 

  • Curatti L, Porchia AC, Herrera-Estrella L, Salerno GL (2000) A prokaryotic sucrose synthase gene (susA) isolated from a filamentous nitrogen-fixing cyanobacterium encodes a protein similar to those of plant. Planta 211:729–735

    Article  PubMed  CAS  Google Scholar 

  • Curatti L, Flores E, Salerno G (2002) Sucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp. FEBS Lett 513:175–178

    Article  PubMed  CAS  Google Scholar 

  • Desplats P, Folco E, Salerno GL (2005) Sucrose may play an additional role to that of an osmolyte in Synechocystis sp PCC 6803 salt-shocked cells. Plant Physiol Biochem 43:133–138

    Article  PubMed  CAS  Google Scholar 

  • Elhai J, Wolk CP (1988) Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754

    Article  PubMed  CAS  Google Scholar 

  • Elhai J, Wolk CP (1990) Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J 9:3379–3388

    PubMed  CAS  Google Scholar 

  • Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33:164–167

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Dominguez M, Reyes JC, Florencio FJ (2000) NtcA represses transcription of gifA and gifB, genes that encode inhibitors of glutamine synthetase type I from Synechocystis sp PCC 6803. Mol Microbiol 35:1192–1201

    Article  PubMed  CAS  Google Scholar 

  • Golden JW, Yoon HS (2003) Heterocyst development in Anabaena. Curr Opin Microbiol 6:557–563

    Article  PubMed  CAS  Google Scholar 

  • Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183:411–425

    Article  PubMed  CAS  Google Scholar 

  • Herrero A, Muro-Pastor AM, Valladares A, Flores E (2004) Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487

    Article  PubMed  CAS  Google Scholar 

  • Jiang F, Mannervik B, Bergman B (1997) Evidence for redox regulation of the transcription factor NtcA, acting both as an activator and a repressor, in the cyanobacterium Anabaena PCC 7120. Biochem J 15:513–517

    Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  PubMed  CAS  Google Scholar 

  • Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56

    Article  PubMed  CAS  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage?. Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • Muro-Pastor AM, Valladares A, Flores E, Herrero A (1999) The hetC gene is a direct target of the NtcA transcriptional regulator in cyanobacterial heterocyst development. J Bacteriol 181:6664–6669

    PubMed  CAS  Google Scholar 

  • Nierzwicki-Bauer SA, Curtis SE, Haselkorn R (1984) Cotranscription of genes encoding the small and large subunits of ribulose−1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 81:5961–5965

    Article  PubMed  CAS  Google Scholar 

  • Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM (2004) Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5:R91

    PubMed  Google Scholar 

  • Pfannschmidt T (2003) Chloroplasts redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  PubMed  CAS  Google Scholar 

  • Porchia AC, Curatti L, Salerno GL (1999) Sucrose metabolism in cyanobacteria: sucrose synthase from Anabaena sp strain PCC 7119 is remarkably different from the plant enzymes with respect to substrate affinity and amino-terminal sequence. Planta 210:34–40

    Article  PubMed  CAS  Google Scholar 

  • Ramasubramanian TS, Wei TF, Golden JW (1994) Two Anabaena sp strain PCC 7120 DNA-binding factors interact with vegetative cell- and heterocyst-specific genes. J Bacteriol 176:1214–1223

    PubMed  CAS  Google Scholar 

  • Rolland F, Sheen J (2005) Sugar sensing and signalling networks in plants. Biochem Soc Trans 33:269–271

    Article  PubMed  CAS  Google Scholar 

  • Salerno GL, Curatti L (2003) Origin of sucrose metabolism in higher plants: when, how and why? Trends Plant Sci 8:63–69

    Article  PubMed  CAS  Google Scholar 

  • Salerno GL, Porchia A, Sánchez N (1995) Biosynthesis of sucrose in lower organisms. In: Pontis HG, Salerno GL, Echeverria EJ (eds) Sucrose metabolism, biochemistry, physiology and molecular biology. Current topics in Plant Physiology Series vol 14. American Society of Plant Physiology, College Park, MD, pp34–39

  • Sambrook J, Russell DW (eds) (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

  • Schilling N, Ehrnsperger K (1985) Cellular differentiation of sucrose metabolism in Anabaena variabilis. Z Naturforsch 40:776–779

    Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81

    Article  PubMed  CAS  Google Scholar 

  • Vioque A (1997) The RNase P RNA from cyanobacteria: short tandemly repeated repetitive (STRR) sequences are present within the RNase P RNA gene in heterocyst-forming cyanobacteria. Nucleic Acids Res 25:3471–3477

    Article  PubMed  CAS  Google Scholar 

  • Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35:253–289

    Article  PubMed  CAS  Google Scholar 

  • Wolk CP, Ernst A, Elhai J (1994) Heterocyst metabolism and development. In: Bryant DA (eds) The molecular biology of cyanobacteria. Kluwer Academic, Dordrecht, pp 769–823

    Google Scholar 

Download references

Acknowledgments

This research was supported by grants of ANPCyT (PICT 12233), CONICET, Universidad Nacional de Mar del Plata and FIBA. We are grateful to J. Golden for facilitating the vectors pAM505 and pKEN-GFPmut2 and the Anabaena sp. strain AMC486, and to H. Pontis and our colleagues at the CIB-FIBA for many helpful discussions.

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Correspondence to Graciela L. Salerno.

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Curatti, L., Giarrocco, L. & Salerno, G.L. Sucrose synthase and RuBisCo expression is similarly regulated by the nitrogen source in the nitrogen-fixing cyanobacterium Anabaena sp.. Planta 223, 891–900 (2006). https://doi.org/10.1007/s00425-005-0142-7

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