Download PDF
Plant Biol (Stuttg) 2004; 6(4): 408-414
DOI: 10.1055/s-2004-820872
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Coordinated Expression of Sulfate Uptake and Components of the Sulfate Assimilatory Pathway in Maize

L. Hopkins1 , S. Parmar1 , D. L. Bouranis2 , J. R. Howarth1 , M. J. Hawkesford1
  • 1Crop Performance and Improvement Division, Rothamsted Research, Harpenden AL5 2JQ, UK
  • 2Plant Physiology Laboratory, Department of Plant Biology, Faculty of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
Further Information

Publication History

Publication Date:
12 July 2004 (online)

   Permissions and Reprints

Abstract

A high-affinity-type sulfate transporter (Group 1: ZmST1;1, Accession No. AF355602) has been cloned from maize seedlings by RT-PCR. Tissue and cell specific localisation of this sulfate transporter has been determined along the developmental gradient of the root and in leaves of different ages. In S-sufficient conditions there was uniform low expression of ZmST1;1 in the root and very low expression in the leaves. Increased mRNA abundance and sulfate influx capacity indicated that S-starvation increased ZmST1;1 expression in roots, especially at the top of the root (just behind the seed, the area possessing most laterals and root hairs) compared to the root tip. Similarly a group 2, probable low affinity-type sulfate transporter, ZmST2;1, and also ATP-sulfurylase and APS-reductase but not OAS(thiol)lyase were induced by S-starvation and showed highest expression in the upper section of the root. S-starvation increased root/shoot ratio by 20 % and increased root lateral length and abundance in the region closest to the root tip. As the increase in root proliferation was not as great as the increase in mRNA pools, it was clear that there was a higher cellular abundance of the mRNAs for sulfate transporters, ATP-sulfurylase, and APS-reductase in response to sulfur starvation. In the leaves, the sulfate transporters, ATP-sulfurylase and APS-reductase were induced by S-starvation with the most mature leaf showing increased mRNA abundance first. In situ hybridization indicated that ZmST1;1 was expressed in epidermal and endodermal cell layers throughout the root whilst OAS(thiol)lyase was highly expressed in the root cortex.

Key words

Sulfate transporter - ATP-sulfurylase - APS-reductase - sulfur assimilation - root morphology - maize

References

  • 1 Bogdanova N., Hell R.. Cysteine synthesis in plants. Protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. .  Plant Journal. (1997);  11 251-262
    CrossrefPubMedSearch in Google Scholar
  • 2 Bolchi A., Petrucco S., Tenca P. L., Foroni C., Ottonello S.. Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine.  Plant Molecular Biology. (1999);  39 527-537
    CrossrefPubMedSearch in Google Scholar
  • 3 Burgener M., Suter M., Jones S., Brunold C.. Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves.  Plant Physiology. (1998);  116 1315-1322
    CrossrefPubMedSearch in Google Scholar
  • 4 Clarkson D. T., Saker L. R., Purves J. V.. Depression of nitrate and ammonium transport in barley plants with diminished sulphate status - evidence of co-regulation of nitrogen and sulphate intake.  Journal of Experimental Botany. (1989);  40 953-963
    PubMedSearch in Google Scholar
  • 5 Clarkson D. T., Hawkesford M. J., Davidian J.-C.. Membrane and long-distance transport of sulfate. de Kok, L. J., Stulen, I., Rennenberg, H., Brunold, C., and Rauser, W. E., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. The Hague, The Netherlands; SPB Academic Publishing (1993): 3-19
    Search in Google Scholar
  • 6 Cram W. J.. Uptake and transport of sulfate. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants: Fundamental, Environmental and Agricultural Aspects (Rennenberg, H., Brunold, C., de Kok, L. J., Stulen, I., eds,).  Uptake and transport of sulfate. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants: Fundamental, Environmental and Agricultural Aspects (Rennenberg, H., Brunold, C., de Kok, L. J., Stulen, I., eds,). The Hague, The Netherlands; SPB Academic Publishing (1990): 3-11
    Search in Google Scholar
  • 7 Droux M., Ruffet M.-L., Douce R., Job D.. Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants. Structural and kinetic properties of the free and bound enzymes.  European Journal of Biochemistry. (1998);  255 235-245
    CrossrefPubMedSearch in Google Scholar
  • 8 Fowler J., Cohen L., Jarvis P.. Practical Statistics for Field Biology, 2nd edition. New York; Wiley (2000)
    Search in Google Scholar
  • 9 Fricker M. D., May M., Meyer M. J., Sheard N., White N. S.. Measurement of glutathione levels in intact roots of Arabidopsis. .  Journal of Microscopy. (2000);  198 162-173
    CrossrefPubMedSearch in Google Scholar
  • 10 Gutierrez-Marcos J., Roberts M. A., Campbell E. I., Wray J. L.. Three members of a novel gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity.  Proceedings of the National Academy of Sciences of the United States of America. (1996);  93 13377-13382
    CrossrefPubMedSearch in Google Scholar
  • 11 Hawkesford M. J.. Transporter gene families in plants: the sulphate transporter gene family - redundancy or specialization?.  Physiologia Plantarum. (2003);  117 155-165
    CrossrefPubMedSearch in Google Scholar
  • 12 Hawkesford M. J., Wray J. L.. Molecular genetics of sulfate assimilation.  Advances in Botanical Research. (2000);  33 160-208
    PubMedSearch in Google Scholar
  • 13 Hell R.. Molecular physiology of plant sulfur metabolism.  Planta. (1997);  202 138-148
    CrossrefPubMedSearch in Google Scholar
  • 14 Hell R., Hillebrand H.. Plant concepts for mineral acquisition and allocation.  Current Opinion in Biotechnology. (2001);  12 161-168
    CrossrefPubMedSearch in Google Scholar
  • 15 Howarth J. R., Fourcroy P., Davidian J.-C., Smith F. W., Hawkesford M. J.. Cloning of two contrasting sulfate transporters from tomato induced by low sulfate and infection by the vascular pathogen Verticillium dahliae. .  Planta. (2003);  218 58-64
    CrossrefPubMedSearch in Google Scholar
  • 16 Kopriva S., Jones S., Koprivova A., Suter M., von Ballmoos P., Brander K., Flückiger J., Brunold C.. Influence of chilling stress on the intercellular distribution of assimilatory sulfate reduction and thiols in Zea mays. .  Plant Biology. (2001);  3 24-31
    Thieme ConnectPubMedSearch in Google Scholar
  • 17 Lappartient A. G., Touraine B.. Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact canola.  Plant Physiology. (1996);  111 147-157
    PubMedSearch in Google Scholar
  • 18 Lappartient A. G., Vidmar J. J., Leustek T., Glass A. D. M., Touraine B.. Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound.  Plant Journal. (1999);  18 89-95
    CrossrefPubMedSearch in Google Scholar
  • 19 Leustek T., Saito K.. Sulfate transport and assimilation in plants.  Plant Physiology. (1999);  120 637-643
    CrossrefPubMedSearch in Google Scholar
  • 20 Leustek T., Martin M. N., Bick J.-A., Davies J. P.. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies.  Annual Reviews in Plant Physiology and Plant Molecular Biology. (2000);  51 141-165
    PubMedSearch in Google Scholar
  • 21 Pearson W. R.. Flexible sequence similarity searching with the FASTA3 program package.  Methods in Molecular Biology. (2000);  132 185-219
    PubMedSearch in Google Scholar
  • 22 Ruffet M.-L., Droux M., Douce R.. Purification and kinetic properties of serine acetyltransferase free of O-acetylserine(thiol)lyase from spinach chloroplasts.  Plant Physiology. (1994);  104 597-604
    PubMedSearch in Google Scholar
  • 23 Saito K.. Regulation of sulfate transport and synthesis of sulfur-containing amino acids.  Current Opinion in Plant Biology. (1999);  3 188-195
    PubMedSearch in Google Scholar
  • 24 Sambrook J., Fritsch E. F., Maniatis T.. Molecular Cloning: A Laboratory Manual, 2nd edition. Cold Spring Harbor; Cold Spring Harbor Laboratory Press (1989)
    Search in Google Scholar
  • 25 Schmidt A., Jäger K.. Open questions about sulfur metabolism in plants.  Annual Reviews in Plant Physiology. (1992);  43 325-349
    PubMedSearch in Google Scholar
  • 26 Schwarzacher T., Heslop-Harrison J. S.. Practical in Situ Hybridisation. Oxford; Bios Scientific Publishers (2000)
    Search in Google Scholar
  • 27 Smith F. W., Ealing P. M., Hawkesford M. J., Clarkson D. T.. Plant members of a family of sulfate transporters reveal functional subtypes.  Proceedings of the National Academy of Sciences of the United States of America. (1995);  92 9373-9377
    PubMedSearch in Google Scholar
  • 28 Smith F. W., Hawkesford M. J., Ealing P. M., Clarkson D. T., Vandenberg P. J., Belcher A. R., Warrilow A. G. S.. Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter.  Plant Journal. (1997);  12 875-884
    CrossrefPubMedSearch in Google Scholar
  • 29 Takahashi H., Asanuma W., Saito K.. Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform.  Journal of Experimental Botany. (1999);  50 1713-1714
    CrossrefPubMedSearch in Google Scholar
  • 30 Takahashi H., Watanabe-Takahashi A., Smith F. W., Blake-Kalff M., Hawkesford M. J., Saito K.. The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. .  Plant Journal. (2000);  23 171-182
    CrossrefPubMedSearch in Google Scholar
  • 31 Takahashi H., Yamazaki M., Sasakura N., Watanabe A., Leustek T., Engler J. D., van Montagu M., Saito K.. Regulation of sulfur assimilation in higher plants: A sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. .  Proceedings of the National Academy of Sciences of the United States of America. (1997);  94 11102-11107
    CrossrefPubMedSearch in Google Scholar
  • 32 Tsakraklides G., Martin M., Chalam R., Tarczynski M. C., Schmidt A., Leustek T.. Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. .  Plant Journal. (2002);  32 879-889
    CrossrefPubMedSearch in Google Scholar
  • 33 Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., von Ballmoos P., Krähenbühl U., Op den Camp R., Brunold C.. Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols.  Plant Journal. (2002);  31 729-740
    CrossrefPubMedSearch in Google Scholar
  • 34 Verwoerd T. C., Dekker B. M., Hoekema A.. A small-scale procedure for the rapid isolation of plant RNAs.  Nucleic Acids Research. (1989);  17 2362
    PubMedSearch in Google Scholar
  • 35 Yamaguchi Y., Nakamura T., Harada E., Koizumi N., Sano H.. Differential accumulation of transcripts encoding sulfur assimilation enzymes upon sulfur and/or nitrogen deprivation in Arabidopsis thaliana. .  Bioscience, Biotechnology and Biochemistry. (1999);  63 762-766
    CrossrefPubMedSearch in Google Scholar

M. J. Hawkesford

Crop Performance and Improvement Division

Rothamsted Research

Harpenden, Hertfordshire, AL5 2JQ

UK

Email: malcolm.hawkesford@bbsrc.ac.uk

Section Editor: H. Rennenberg