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

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.

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
• 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
• 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
• 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
• 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
• 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
• 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
• 8 Fowler J., Cohen L., Jarvis P.. Practical Statistics for Field Biology, 2nd edition. New York; Wiley (2000)
• 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
• 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
• 11 Hawkesford M. J.. Transporter gene families in plants: the sulphate transporter gene family - redundancy or specialization?.  Physiologia Plantarum. (2003);  117 155-165
• 12 Hawkesford M. J., Wray J. L.. Molecular genetics of sulfate assimilation.  Advances in Botanical Research. (2000);  33 160-208
• 13 Hell R.. Molecular physiology of plant sulfur metabolism.  Planta. (1997);  202 138-148
• 14 Hell R., Hillebrand H.. Plant concepts for mineral acquisition and allocation.  Current Opinion in Biotechnology. (2001);  12 161-168
• 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
• 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
• 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
• 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
• 19 Leustek T., Saito K.. Sulfate transport and assimilation in plants.  Plant Physiology. (1999);  120 637-643
• 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
• 21 Pearson W. R.. Flexible sequence similarity searching with the FASTA3 program package.  Methods in Molecular Biology. (2000);  132 185-219
• 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
• 23 Saito K.. Regulation of sulfate transport and synthesis of sulfur-containing amino acids.  Current Opinion in Plant Biology. (1999);  3 188-195
• 24 Sambrook J., Fritsch E. F., Maniatis T.. Molecular Cloning: A Laboratory Manual, 2nd edition. Cold Spring Harbor; Cold Spring Harbor Laboratory Press (1989)
• 25 Schmidt A., Jäger K.. Open questions about sulfur metabolism in plants.  Annual Reviews in Plant Physiology. (1992);  43 325-349
• 26 Schwarzacher T., Heslop-Harrison J. S.. Practical in Situ Hybridisation. Oxford; Bios Scientific Publishers (2000)
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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

Section Editor: H. Rennenberg