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Molecular biological approaches to plant nutrition

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Abstract

In the last decade, understanding of ion transport has grown sufficiently to pose sensible questions about the molecular nature of the processes and their regulation. Techniques for identifying and cloning genes and for genetic transformation provide the means for answering these questions.

Transport of ions across membranes is obviously a major aspect of mineral nutrition since it occurs during initial absorption, compartmentation and mobilisation of nutrients. Here, we will briefly review the types of transport protein involved and show how molecular biology and recombinant DNA technology have revealed something of their structure. Strategies used to identify the genes for transporters are discussed and reference is made to areas in which the availability of cloned genes will facilitate future studies.

Mineral nutrition involves, however, more than membrane transport. The absorption rates of major nutrients are quite strictly regulated by biochemical factors which vary with the rate at which nutrients are used in growth. Nitrogen, sulphur and phosphate nutrition in micro-organisms are regulated by the interaction of various DNA-binding proteins with the promoter regions of genes for key enzymes in the assimilatory pathways and the specific ion permeases. The expression of the regulatory protein or its activity can be modified by metabolites, such as glutamine. Some evidence supports the idea that higher plants also have groups of genes with a common regulation of expression.

An attempt is made to identify some reasonable objectives, which should increase understanding of the regulation of nutrient transport.

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Abbreviations

cDNA:

complementary strand of DNA prepared from a messenger RNA

NR:

nitrate reductase

NiR:

nitrite reductase

Pi :

inorganic phosphate

PPase:

pyrophosphate

RUBISCO:

rubulose bisphosphate carboxylase oxygenase. Genes are referred to as follows e.g. cys-3 and scon-1. The protein products of these genes, where they have no familiar name are referred to as CYS3 and SCON-1 respectively

References

  • Anderson J A, Huprikar S S, Kochian L V, Lucas W J and Gaber R F 1992 Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89, 3736–3740.

    PubMed  Google Scholar 

  • Aslam M, Travis R L and Huffaker R C 1992 Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiol. 99, 1124–1133.

    PubMed  Google Scholar 

  • Boorer K J, Forde B G, Leigh R A and Miller A J 1992 Functional expression of a plant plasma membrane transporter in Xenopus oocytes. FEBS Letters 302, 166–168.

    Article  PubMed  Google Scholar 

  • Chapin F SIII 1980. The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11, 233–260.

    Article  Google Scholar 

  • Chapin F SIII, Walter C H S and Clarkson D T 1988 Growth response of barley and tomato to nitrogen stress and its control by abscisic acid, water relations and photosynthesis. Planta 173, 352–366.

    Article  Google Scholar 

  • Clarkson D T and Lüttge U 1991 Mineral nutrition: inducible and repressible nutrient transport systems. Progress in Bot. 52, 61–83, Springer-Verlag, Berlin, Heidelberg.

    Google Scholar 

  • Clarkson D T, Hawkesford M J, Davidian J-C and Grignon C 1992 Contrasting responses of sulphate and phosphate transport in barley (Hordeum vulgare L.) roots to protein-modifying reagents and inhibition of protein synthesis. Planta 187, 306–314.

    Article  Google Scholar 

  • Clausen S and Apel K 1991 Seasonal changes in the concentration of the major storage protein and its mRNA in xylem ray cells of poplar trees. Plant Mol. Biol. 17, 669–678.

    PubMed  Google Scholar 

  • van Cleve B and Apel K 1993 Induction by nitrogen and low temperature of storage-protein synthesis in poplar trees exposed to long days. Planta 189, 157–160.

    Google Scholar 

  • Cogliatti D H and Clarkson D T 1983 Physiological changes in potato plants during development of, and recovery from phosphate stress. Physiol. Plant. 58, 287–294.

    Google Scholar 

  • Cogliatti D H and Santa Maria G E 1990 Influx and efflux of P in roots of wheat plants in non-growth-limiting P concentrations. J. Exp. Bot. 41, 601–607.

    Google Scholar 

  • Cram W J 1990 Uptake and transport of sulfate. In Sulfur Nutrition and Sulfur assimilation in Higher Plants. Ed. H Rennenberg, Ch Brunold, L J DeKok and I Stulen, pp 3–11. SPB Publishing, The Hague.

    Google Scholar 

  • Deane-Drummond C E and Glass A D M 1983 Short term studies of nitrate uptake into barley plants using ion-specific electrodes and 36CIO3 efflux. Plant Physiol. 73, 100–104.

    Google Scholar 

  • Dhugga K S, Waines J G and Leonard R T 1988 Correlated induction of nitrate uptake and membrane polypeptides in corn roots. Plant Physiol. 87, 120–125.

    Google Scholar 

  • Duarte P J P and Larsson C-M 1993 Translocation of nutrients into N-limited, non-nodulated pea plants. J. Plant Physiol. 141, 182–187.

    Google Scholar 

  • Dudler R and Hertig C 1992 Structure of an mdr-like gene from Arabidopsis thaliana. J. Biol. Chem. 267, 5882–5888.

    PubMed  Google Scholar 

  • Dunn-Coleman N S, Smarrelli JJr and Garrett R H 1984 Nitrate assimilation in eukaryotic cells. Int. Rev. Cytol. 92, 1–50.

    Google Scholar 

  • Ferreira R M B and Teixeira A R N 1992 Sulfur starvation in Lemna leads to degradation of ribulose bisphosphate carboxylase without plant death. J. Biol. Chem. 267, 7253–7257.

    PubMed  Google Scholar 

  • Flügge U I, Weber A, Fischer K, Lottspeich F, Eckerskorn C, Waegermann K and Soll J 1991 The major chloroplast envelope polypeptide is the phosphate translocator and not the protein import receptor. Nature 353, 364–367.

    Google Scholar 

  • Fu Y-H and Marzluf G A 1992 cys-3, the positive-acting sulfur regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. J. Biol. Chem. 265, 11942–11947.

    Google Scholar 

  • Fu Y-H, Lee H-J, Young J L, Jarai G and Marzluf G A 1990. Nitrogen and sulfur regulatory circuits of Neurospora. In Developmental Biology. pp. 319–335. Wiley-Liss, NY.

    Google Scholar 

  • Glass A D M 1983 Regulation of ion transport. Ann. Rev. Plant Physiol. 34, 311–326.

    Google Scholar 

  • Goldstein A H, Baertelin D A and McDaniel R G 1988a Phosphate starvation inducible metabolism in Lycopersicon esculentum. I. Excretion of acid phosphatase by tomato plants and suspension cultured cells. Plant Physiol. 87, 711–715.

    Google Scholar 

  • Goldstein A H, Danon A, Baertelin D A and McDaniel R G 1988b Phosphate starvation inducible metabolism in Lycopersicon esculentum. II. Characterization of the phosphate starvation inducible-excreted acid phosphatase. Plant Physiol. 87, 716–720.

    Google Scholar 

  • Goldstein A H, Mayfield S P, Danon A and Tibbot B K 1989 Phosphate starvation inducible metabolism in Lycopersicon esculentum. III. Changes in protein secretion under nutrient stress. Plant Physiol. 91, 175–182.

    Google Scholar 

  • Graham R D 1984 Breeding for nutritional characteristics in cereals. Advan. Plant Nutrit. 1, 57–102.

    Google Scholar 

  • Green D G, Ferguson W S and Warder F G 1973 Accumulation of toxic levels of phosphorus in the leaves of phosphorus-deficient barley. Can. J. Plant Sci. 53, 241–246.

    Google Scholar 

  • Green L S, Laudenbach D E and Grossman A R 1989 A region of cyanobacterial genome required for sulfate transport. Proc. Natl. Acad. Sci. USA 86, 1949–1953.

    PubMed  Google Scholar 

  • Greenwood J S, Demmers C and Wetzel S 1990 Seasonally dependent formation of protein-storage vacuoles in the inner bark tissues of Salix microstachya. Can. J. Bot. 68, 1747–1755.

    Google Scholar 

  • Griffith J K, Baker M E, Rouch D A, Page M G P, Skurray R A, Paulsen I T, Chater K F, Baldwin S A and Henderson P J F 1992 Membrane transport proteins: implications of sequence comparisons. Current Opinion in Cell Biology, 4, 684–695.

    Google Scholar 

  • Grove G and Marzluf G A 1981 Identification of the produc, of the major regulatory gene of the nitrogen control circuit of Neurospora crassa as a nuclear DNA-binding protein. J. Biol. Chem. 256, 463–470.

    PubMed  Google Scholar 

  • Harper J F, Surowy T K and Sussman M R 1989 Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 86, 1234–1238.

    PubMed  Google Scholar 

  • Hawkesford M J and Belcher A R 1991 Differential protein synthesis in response to sulphate and phosphate deprivation: Identification of possible components of plasma-membrane transport systems in cultured tomato roots. Planta 185, 323–329.

    Article  Google Scholar 

  • Hawkesford M J, Davidian J-C and Grignon C 1993 Sulphate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L.: increased transport in membranes isolated from sulphur-starved plants. Planta 190, 297–304.

    Article  Google Scholar 

  • Hocking P J and Meyer C P 1991a Effects of CO2-enrichmem and nitrogen stress on growth, partitioning of dry matter and nitrogen in wheat and maize. Aust. J. Plant Physiol. 18, 339–356.

    Google Scholar 

  • Hocking P J and Meyer C P 1991b Carbon dioxide enrichment decreases critical nitrate and total nitrogen concentration in wheat. J. Plant Nutrit. 14, 571–584.

    Google Scholar 

  • Johnson K D, Höfte H and Chrispeels M J 1990 An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a baterial solute transporter (GlpF). Plant Cell 2, 525–532.

    Article  PubMed  Google Scholar 

  • Jarai G, Truong H-W, Daniel-Vedele F and Marzluf G A 1992 NIT2, the nitrogen regulatory protein of Neurospora crassa, binds upstream of nia, the tomato nitrate reductase gene, in vitro. Curr. Genetics 21, 37–41.

    Article  Google Scholar 

  • Kaback H R 1990 Lac permease of Escherichia coli: on the path of the proton. Phil. Trans. R. Soc. Lond. B 326, 425–436.

    Google Scholar 

  • Ketter J S, Jarai G, Fu Y H and Marzluf G A 1991 Nucleotide-sequence, messenger-RNA stability and DNA recognition elements of CYS-14, the structural gene for sulfate permease-II in Neurospora crassa. Biochemistry 30, 1780–1787.

    PubMed  Google Scholar 

  • Lee R B, Ratcliffe R G and Southon T E 1990 31P NMR measurements of cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes. J. Exp. Bot. 41, 1063–1078.

    Google Scholar 

  • Marschner H 1991 Root-induced changes in the availability of micronutrients in the rhizosphere. In Plant Roots, the Hidden Half. Eds. Y Waisel, A Eshel and U Kafkafi. pp 503–528. M Dekker, New York.

    Google Scholar 

  • McClure P R, Omholt T E, Pace G M, and Bouthyette P-Y 1987 Nitrate-induced changes in protein synthesis and translation of RNA in maize roots. Plant Physiol. 84, 52–57.

    Google Scholar 

  • Millard P 1988 The accumulation and storage of nitrogen by herbaceous plants. Plant Cell Environment 11, 108.

    Google Scholar 

  • Millard P and Catt J W 1988 The Influence of nitrogen supply on the use of nitrate and ribulose 1,5 bisphosphate carboxylase/oxygenase as leaf nitrogen stores for growth of potato tubers (Solanum tuberosum L.). J. Exp. Bot. 39, 1–11.

    Google Scholar 

  • Millard P and Proe M F 1991 Leaf demography and seasonal internal cycling on nitrogen in sycamore (Acer pseudoplatanus L.) seedlings in relation to nitrogen supply. New Phytol. 117, 587–596.

    Google Scholar 

  • Neininger A, Bichler J, Schneiderbauer A and Mohr H 1993 Responses of a nitrite-reductase 3.1 kilobase upstream regulatory sequence from spinach to nitrate and light in transgenic tobacco. Planta 189, 440–442.

    Google Scholar 

  • Pardo J M and Serrano R 1989 Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J. Biol. Chem. 264, 8557–8562.

    PubMed  Google Scholar 

  • Paietta J V, Atkins R A, Lambowitz A M and Marzluf G A 1987 Molecular cloning and characterization of the CYS-3 regulatory protein of Neurospora crassa. Mol. Cell Biol. 7, 2506–2511.

    Google Scholar 

  • Quick W P, Schurr U, Scheibe R, Schultz E-D, Rodermel S R, Bogorad L and Stitt M 1991. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with "antisense" rbc5. I. Impact on photosynthesis in ambient growth conditions. Planta 183, 542–554.

    Article  Google Scholar 

  • Quick W P, Fichtner K, Schulze E-D, Wendler R, Leegood R C, Mooney H, Rodermel S R, Bogorad L and Stitt M 1992 Decreased ribulose-1,5-bisphosphate carboxylase oxygenase in transgenic tobacco transformed with "antisense" rbc5. IV Impact on photosynthesis in conditions of altered nitrogen supply. Planta 188, 522–531.

    Article  Google Scholar 

  • Rea P A, Kim Y, Sarafian V, Poole R J and Britten CJ 1992 Vacuolar H+-translocating inorganic pyrophosphatase biochemistry and molecular biology. In: Transport and Receptor Proteins of Plant Membranes (Eds Cooke DT and Clarkson DT). Plenum Press, New York, pp. 25–38.

    Google Scholar 

  • Redinbaugh M G and Campbell W H 1991. Higher plant responses to environmental nitrate. Physiol Plant. 82, 640–650.

    Article  Google Scholar 

  • Rennenberg H, Kemper O and Theone B 1989 Recovery of sulfate transport in heterotrophic tobacco cells from inhibition by reduced glutathione. Physiol. Plant. 76, 271–276.

    Google Scholar 

  • Riesmeier J W, Willmitzer L and Frommer W B 1992 Isolation and characterisation of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO Journal 11, 4705–4713.

    PubMed  Google Scholar 

  • Rodermel S R, Abbott M S and Bogorad L 1988 Nuclearorganelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55, 673–681.

    Article  PubMed  Google Scholar 

  • Sauer N, Caspari T, Klebl F and Tanner W 1990a Functional expression of the Chlorella hexose transporter in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 87, 7949–7952.

    PubMed  Google Scholar 

  • Sauer N, Friedländer K and Gräml-Wicke U 1990b Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO Journal 9, 3045–3050.

    PubMed  Google Scholar 

  • Schachtman D P, Schoeder J I, Lucas W J, Anderson J A and Gaber R F 1992 Expression of inward-rectifying potassium channel by Arabisopsis KAT1 cDNA. Science 258, 1654–1658.

    PubMed  Google Scholar 

  • Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon J-M, Gaymard F and Grignon C 1992 Cloning and expression in yeast of a plant potassium ion transport system. Science 256, 663–665.

    PubMed  Google Scholar 

  • Shinigawa H, Makino K, Amemura M and Nakata A 1987 Structure and function of regulatory genes for the phosphate regulon of Escherichia coli. In Phosphate Metabolism and Cellular Regulation in Micro-organisms. Ed. A Torriani-Gorini, F G Rothman, S Silver, A Wright and E Yagil. pp 20–25. Amer. Sci. Microbiol., Washington.

    Google Scholar 

  • Staswick P E 1990 Novel regulation of vegetative storage protein genes. The Plant Cell 2, 1–6.

    Article  PubMed  Google Scholar 

  • Tsay Y-F, Schroeder J I, Feldmann K A and Crawford N M 1993 The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705–712.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Agricultural Sciences, University of Bristol, AFRC Institute of Arable Crops Research, Long Ashton Research Station, BS18 9AF, Bristol, UK

    David T. Clarkson & Malcolm J. Hawkesford

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  1. David T. Clarkson
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  2. Malcolm J. Hawkesford
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Clarkson, D.T., Hawkesford, M.J. Molecular biological approaches to plant nutrition. Plant Soil 155, 21–31 (1993). https://doi.org/10.1007/BF00024981

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