The Characteristic High Sulfate Content in Brassica oleracea is Controlled by the Expression and Activity of Sulfate Transporters

Abstract

The uptake and distribution of sulfate in Brassica oleracea, a species characterised by its high sulfate content in root and shoot, are coordinated and adjusted to the sulfur requirement for growth, even at external sulfate concentrations close to the K_m value of the high-affinity sulfate transporters. Plants were able to grow normally and maintain a high sulfur content when grown at 5 or 10 µM sulfate in the root environment. Abundance of mRNAs for the high affinity sulfate transporters, BolSultr1;1 and BolSultr1;2, were enhanced at ≤ 25 µM sulfate, and this was accompanied with an up to three-fold increase in the sulfate uptake capacity, whereas sulfate, organic sulfur, and thiol contents were only slightly affected. Upon sulfate deprivation, there was a much greater induction of the sulfate transporters, BolSultr1;1, BolSultr1;2, BolSultr1;3, BolSultr2;1, and BolSultr4;1, whilst the sulfate uptake capacity was only increased up to four-fold. Plant growth and shoot to root biomass allocation were affected only upon sulfate-deprivation and not at low external sulfate concentrations. From the current results it is suggested that the internal sulfate concentration may act as a determining factor in the regulation of activity and expression of sulfate transporters, and of shoot to root biomass allocation in B. oleracea.

Key words

Brassica oleracea - sulfate deprivation - sulfate transporters - sulfate uptake - sulfur assimilation - sulfur deficiency - sulfur metabolism - Sultr.

References

• 1 Buchner P., Stuiver C. E. E., Westerman S., Wirtz M., Hell R., Hawkesford M. J., De Kok L. J.. Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea L. as affected by atmospheric H₂S and pedospheric sulfate nutrition.  Plant Physiology. (2004);  136 3396-3408
• 2 Castro A., Aires A., Rosa E., Bloem E., Stulen I., De Kok L. J.. Distribution of glucosinolates in Brassica oleracea cultivars.  Phyton. (2004);  44 133-143
• 3 Castro A., Stulen I., De Kok L. J.. Nitrogen and sulfur requirement of Brassica oleracea L. cultivars. Davidian, J.-C., ed. Sulfur Transport and Assimilation in Plants. Regulation, Interaction and Signaling. Leiden; Backhuys Publishers (2003): 181-183
• 4 Church G. M., Gilbert W.. Genomic sequencing.  Proceedings of the National Academy of Sciences of the USA. (1984);  81 1991-1995
• 5 Clarkson D. T., Hawkesford M. J., Davidian J.-C.. Membrane and long-distance transport of sulfate. De Kok, L. J., ed. Sulfur Nutrition and Assimilation in Higher Plants: Regulatory, Agricultural and Environmental Aspects. The Hague; SPB Academic Publishing (1993): 3-19
• 6 Clarkson D. T., Saker L. R.. Sulphate influx in wheat and barley roots becomes more sensitive to specific protein-binding reagents when plants are sulphate-deficient.  Planta. (1989);  178 249-257
• 7 Clarkson D. T., Smith F. W., Vanden Berg P. J.. Regulation of sulphate transport in a tropical legume, Macroptilium atropurpureum, cv. Siratro.  Journal of Experimental Botany. (1983);  34 1463-1483
• 8 Davidian J.-C., Hatzfeld Y., Cathala N., Tagmount A., Vidmar J. J.. Sulfate uptake and transport in plants. Brunold, C., ed. Sulfur Nutrition and Sulfur Assimilation in Higher Plants: Molecular, Biochemical and Physiological Aspects. Bern; Paul Haupt (2000): 19-40
• 9 De Kok L. J., Buwalda F., Bosma W.. Determination of cysteine and its accumulation in spinach leaf tissue upon exposure to excess sulfur.  Journal of Plant Physiology. (1988);  133 502-505
• 10 De Kok L. J., Castro A., Durenkamp M., Stuiver C. E. E., Westerman S., Yang L., Stulen I.. Sulphur in plant physiology. Proceedings 500. York; International Fertilizer Society (2002): 1-26
• 11 Durenkamp M., De Kok L. J.. Impact of pedospheric and atmospheric sulphur nutrition on sulphur metabolism of Allium cepa L., a species with a potential sink capacity for secondary sulphur compounds.  Journal of Experimental Botany. (2004);  55 1821-1830
• 12 Durenkamp M., De Kok L. J., Kopriva S.. Adenosine 5′-phosphosulphate reductase is regulated differently in Allium cepa L. and Brassica oleracea L. upon exposure to H₂S.  Journal of Experimental Botany. (2007);  DOI: 10.1093/jxb/erm031
• 13 Ernst W. H. O.. Ecological aspects of sulfur metabolism. Rennenberg, H., ed. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Fundamental, Environmental and Agricultural Aspects. The Hague; SPB Academic Publishing (1990): 131-144
• 14 Haneklaus S., Bloem E., Schnug E.. Sulfur interactions in crop ecosystems. Hawkesford, M. J. and De Kok, L. J., eds. Sulfur in Plants. An Ecological Perspective. Dordrecht; Springer (2007 a): 17-58
• 15 Haneklaus S., Bloem E., Schnug E., De Kok L. J., Stulen I.. Sulfur. Baker, A. V. and Pilbeam, D. J., eds. Handbook of Plant Nutrition. Boca Raton; Taylor and Francis (2007 b): 183-238
• 16 Hawkesford M. J.. Transporter gene families in plants: the sulfate transporter gene family - redundancy or specialization?.  Physiologia Plantarum. (2003);  117 155-163
• 17 Hawkesford M. J.. Sulfur and plant ecology: a central role of sulfate transporters for responding to sulfur availability. Hawkesford, M. J. and De Kok, L. J., eds. Sulfur in Plants. An Ecological Perspective. Dordrecht; Springer (2007): 1-15
• 18 Hawkesford M. J., De Kok L. J.. Managing sulphur metabolism in plants.  Plant, Cell and Environment. (2006);  29 382-395
• 19 Hawkesford M. J., Wray J. L.. Molecular genetics of sulphur assimilation.  Advances in Botanical Research. (2000);  33 159-223
• 20 Hawkesford M. J., Buchner P., Hopkins L., Howarth J. R.. The plant sulfate transporter family: specialized functions and integration with whole plant nutrition. Davidian, J.-C., ed. Sulfur Transport and Assimilation in Plants. Regulation, Interaction and Signaling. Leiden; Buckhuys Publishers (2003): 1-10
• 21 Hermans Ch., Hammond J. P., White P. J., Verbruggen N.. How do plants respond to nutrient shortage by biomass allocation.  Trends in Plant Science. (2007);  11 610-617
• 22 Herschbach C., Rennenberg H.. Influence of glutathione (GSH) on net uptake of sulphate and sulphate transport in tobacco plants.  Journal of Experimental Botany. (1994);  45 1069-1076
• 23 Herschbach C., van der Zalm E., Schneider A., Jouanin L., De Kok L. J., Rennenberg H.. Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H₂S.  Plant Physiology. (2000);  124 461-473
• 24 Hopkins L., Parmar S., Blaszczyk A., Hesse H., Hoefgen R., Hawkesford M. J.. O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato.  Plant Physiology. (2005);  138 433-440
• 25 Howarth J., Fourcroy P., Davidian J.-C., Smith F. W., Hawkesford M. J.. Cloning of two contrasting high-affinity sulphate transporters from tomato induced by low sulphate and infection by the vascular pathogen Verticillium dahlia.  Planta. (2003);  218 58-64
• 26 Kataoka T., Watanabe-Takahashi A., Hayashi N., Ohnishi M., Mimura T., Buchner P., Hawkesford M. J., Yamaya T., Takahashi H.. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis.  Plant Cell. (2004);  16 2693-2704
• 27 Kronzucker H. J., Siddiqi M. Y., Glass A. D. M.. Compartmentation and flux characteristics of nitrate in spruce.  Planta. (1995);  196 674-682
• 28 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
• 29 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.  The Plant Journal. (1999);  18 89-95
• 47 Leggett J. E., Epstein E.. Kinetics of sulfate absorption by barley roots.  Plant Physiology. (1956);  31 222-226
• 30 Rennenberg H., Kemper O., Thoene B.. Recovery of sulfate transport into heterotrophic tobacco cells from inhibition by reduced glutathione.  Physiologia Plantarum. (1989);  76 271-276
• 31 Saito K.. Sulfur assimilatory metabolism. The long and smelling road.  Plant Physiology. (2004);  136 2443-2450
• 32 Shibagaki N., Rose A., McDermott J. P., Fujiwara T., Hayashi H., Yoneyama T., Davies J. P.. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots.  The Plant Journal. (2002);  29 475-486
• 33 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 USA. (1995);  92 9373-9377
• 34 Smith F. W., Hawkesford M. J., Ealing P. M., Clarkson D. T., van den Berg P. J., Belcher A. R., Warrilow A. G. S.. Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter.  The Plant Journal. (1997);  12 875-884
• 35 Stuiver C. E. E., De Kok L. J., Westerman S.. Sulfur deficiency in Brassica oleracea L.: Development, biochemical characterization, and sulfur/nitrogen interactions.  Russian Journal of Plant Physiology. (1997);  44 505-513
• 36 Takahashi H., Watanabe-Takahashi A., Smith F. W., Blake-Kalff M., Hawkesford M. J., Saito K.. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana.  The Plant Journal. (2000);  23 171-182
• 37 Takahashi H., Yamazaki M., Sasakura N., Watanabe A., Leustek T., de Almeida-Engler J., Engler G., van Montagu M., Saito K.. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate deprived roots plays a central role in Arabidopsis thaliana.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 11102-11107
• 38 van der Zalm E., Schneider A., Rennenberg H.. Regulation of sulfate uptake and xylem loading of poplar roots (Populus tremula × P. alba).  Trees. (2005);  19 204-212
• 39 Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., von Ballmoos P., Krahenbuhl 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.  The Plant Journal. (2002);  31 729-740
• 40 Vidmar J. J., Tagmount A., Cathala N., Touraine B., Davidian J.-C. E.. Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana.  FEBS Letters. (2000);  475 65-69
• 41 Westerman S., Blake-Kalff M. M. A., De Kok L. J., Stulen I.. Sulfate uptake and utilization by two varieties of Brassica oleracea with different sulfur need as affected by atmospheric H₂S.  Phyton. (2001 a);  41 49-62
• 42 Westerman S., Stulen I., Suter M., Brunold C., De Kok L. J.. Atmospheric H₂S as sulfur source for Brassica oleracea: consequences for the activity of the enzymes of the assimilatory sulfate reduction pathway.  Plant Physiology and Biochemistry. (2001 b);  39 425-432
• 43 Yang L., Stulen I., De Kok L. J.. Sulfur dioxide: relevance of toxic and nutritional effects for Chinese cabbage.  Environmental and Experimental Botany. (2006 a);  57 236-245
• 44 Yang L., Stulen I., De Kok L. J.. Impact of sulfate nutrition on the utilization of atmospheric SO₂ as sulfur source for Chinese cabbage.  Journal of Plant Nutrition and Soil Science. (2006 b);  169 529-534
• 45 Yoshimoto N., Inoue E., Saito K., Yamaya T., Takahashi H.. Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis.  Plant Physiology. (2003);  131 1511-1517
• 46 Yoshimoto N., Takahashi H., Smith F. W., Yamaya T., Saito K.. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots.  The Plant Journal. (2002);  29 465-473

Guest Editor: T. Rausch