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Nitrogen nutrition influences some biochemical responses to iron deficiency in tolerant and sensitive genotypes of Vitis

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Abstract

The effects of nitrogen source on iron deficiency responses were investigated in two Vitis genotypes, one tolerant to limestone chlorosis Cabernet Sauvignon (Vitis vinifera cv.) and the other susceptible Gloire de Montpellier (Vitis riparia cv.). Plants were grown with or without Fe(III)-EDTA, and with NO −3 alone or a mixture of NO −3 and NH +4 . Changes in pH of the nutrient solution and root ferric chelate reductase (FC-R) activity were monitored over one week. We carried out quantitative metabolic profiling (1H-NMR) and determined the activity of enzymes involved in organic acid metabolism in root tips. In iron free-solutions, with NO −3 as the sole nitrogen source, the typical Fe-deficiency response reactions as acidification of the growth medium and enhanced FC-R activity in the roots were observed only in the tolerant genotype. Under the same nutritional conditions, organic acid accumulation (mainly citrate and malate) was found for both genotypes. In the presence of NH4+, the sensitive genotype displayed some decrease in pH of the growth medium and an increase in FC-R activity. For both genotypes, the presence of NH + 4 ions decreased significantly the organic acid content of roots. Both Vitis genotypes were able to take up NH +4 from the nutrient solution, regardless of their sensitivity to iron deficiency. The presence of N-NH +4 modified typical Fe stress responses in tolerant and sensitive Vitis genotypes.

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Abbreviations

2OG:

2-oxoglutarate

BPDS:

bathophenanthrolinedisulfonic acid disodium salt hydrate

BSA:

bovine serum albumin

CoA:

coenzyme A

DEA:

diethanolamine

DTNB:

5-5′-dithio-bis-2-nitrobenzoic acid

DTT:

DL-dithiothreitol

EDTA:

ethylenediaminetetracetic acid

ERETIC:

electronic reference to access in vivo concentrations

FW:

fresh weight

GOGAT:

glutamate synthetase

GS:

glutamine synthetase

MDH:

malate dehydrogenase

MES:

2-(N-morpholino)ethanesulfonic acid

NMR:

nuclear magnetic resonance

PEP:

phosphoenolpyruvate

PEPC:

phosphoenolpyruvate carboxylase

PMSF:

phenylmethylsulfonyl fluoride

PVPP:

polyvinylpolypyrrolidone

TCA:

tricarboxylic acid

TEA:

triethylamine

TSP:

(trimethyl) propionic-2,3,3,3-d4 acid sodium salt

References

  • Abadía J, López-Millán A-F, Rombolà A, Abadía A (2002) Organic acids and Fe deficiency: a review. Plant Soil 241:75–86

    Article  Google Scholar 

  • Agnolon F, Santi S, Varanini Z, Pinton R (2001) Enzymatic responses of cucumber roots to different levels of Fe supply. Plant Soil 241:35–41

    Article  Google Scholar 

  • Akoka S, Barantin L, Trierweiler M (1999) Concentration measurement by proton NMR using the ERETIC method. Anal Chem 71:2554–2557

    Article  CAS  Google Scholar 

  • Aktas M, Van Egmond F (1979) Effect of nitrate nutrition on iron utilization by an Fe-efficient and an Fe-inefficient soybean cultivar. Plant Soil 51:257–274

    Article  CAS  Google Scholar 

  • Álvarez-Fernández A, Abadía J, Abadía A (2006) Iron deficiency, fruit yield and fruit quality. In: Barton LL, Abadía J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, the Netherlands, pp 85–101

    Chapter  Google Scholar 

  • Andaluz S, López-Millán A-F, Peleato ML, Abadía J, Abadía A (2002) Increases in phosphoenolpyruvate carboxylase activity in iron-deficient beet roots: analysis of spatial localization and post-translational modification. Plant Soil 241:43–48

    Article  CAS  Google Scholar 

  • Bavaresco L, Fregoni M, Fraschini P (1991) Investigations on iron uptake and reduction by excised roots of different grapevine rootstocks and a V. vinifera cultivar. Plant Soil 130:109–113

    Article  CAS  Google Scholar 

  • Bienfait HF (1996) Is there a metabolic link between H+ excretion and ferric reduction by roots of Fe-deficient plants? A viewpoint. J Plant Nutr 19:1211–1222

    CAS  Google Scholar 

  • Bienfait HF, Bino RJ, Bliek JF, Duivenvoorden JF, Fontaine JM (1983) Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris. Plant Physiol 59:196–202

    Article  CAS  Google Scholar 

  • Brancadoro L, Rabotti G, Scienza A, Zocchi G (1995) Mechanisms of Fe-efficiency in roots of Vitis spp. in response to iron deficiency stress. Plant Soil 171:229–234

    Article  CAS  Google Scholar 

  • Briat J-F, Lobréaux S (1997) Iron transport and storage in plants. Trends Plant Sci 2:187–193

    Article  Google Scholar 

  • Brown JC, Tiffin LO (1965) Iron stress as related to the iron and citrate occurring in stem exudate. Plant Physiol 40:395–400

    PubMed  CAS  Google Scholar 

  • Delhaize E, Ryan PR, Hocking PJ, Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations and citrate efflux from tobacco (Nicotiana tabacum L.) roots. Plant Soil 248:137–144

    Article  CAS  Google Scholar 

  • Dell’Orto M, Brancadoro L, Scienza A, Zocchi G (2000a) Use of biochemical parameters to select grapevine genotypes resistant to iron-chlorosis. J Plant Nutr 23:1767–1775

    CAS  Google Scholar 

  • Dell’Orto M, Santi S, Nisi PD, Cesco S, Varanini Z, Zocchi G, Pinton R (2000b) Development of Fe-deficiency responses in cucumber (Cucumis sativus L.) roots: involvement of plasma membrane H+ ATPase activity. J Exp Bot 51:695–701

    Article  CAS  Google Scholar 

  • Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54:585–593

    Article  PubMed  CAS  Google Scholar 

  • Gogorcena Y, Abadía J, Abadía A (2000) Induction of in vivo root ferric chelate reductase activity in fruit tree rootstock. J Plant Nutr 23:9–21

    CAS  Google Scholar 

  • Gogorcena Y, Molias N, Larbi A, Abadía J, Abadía A (2001) Characterization of the responses of cork oak (Quercus suber) to iron deficiency. Tree Physiol 21:1335–1340

    PubMed  CAS  Google Scholar 

  • Goldberg DM, Ellis G (1974) Isocitrate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie/Academic Press, New York, pp 183–189

    Google Scholar 

  • Gruber B, Kosegarten H (2002) Depressed growth of non-chlorotic vine grown in calcareous soil is an iron deficiency symptom prior to leaf chlorosis. J Plant Nutr Soil Sci 165:111–117

    Article  CAS  Google Scholar 

  • Hodges M, Flesh V, Galvez S, Bismuth E (2003) Higher plant NADP+-dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol Biochem 41:577–585

    Article  CAS  Google Scholar 

  • Hunter JJ, Ruffner HP (1997) Diurnal and seasonal changes in nitrate reductase activity and nitrogen content of grapevines: effect of canopy management. Vitis 36:1–6

    CAS  Google Scholar 

  • Keller M, Kummer M, Carmo Vasconcelos M (2001) Soil nitrogen utilization for growth and gas exchange by grapevines in response to nitrogen supply and rootstock. Aust J Grape Wine Res 7:2–11

    CAS  Google Scholar 

  • Korcak RF (1987) Iron deficiency chlorosis. In: Janick J (ed) Horticultural review. Van Nostrand Reinhold Company, New York, pp 133–186

    Google Scholar 

  • Kosegarten H, Schwed U, Wilson G, Mengel K (1998) Comparative investigation on the susceptibility of faba bean (Vicia faba L.) and sunflower (Helianthus annuus L.) to iron chlorosis. J Plant Nutr 21:1511–1528

    CAS  Google Scholar 

  • Kosegarten H, Hoffmann B, Rroco E, Grolig F, Glüsenkamp K-H, Mengel K (2004) Apoplastic pH and FeIII reduction in young sunflower (Helianthus annuus) roots. Physiol Plant 122:95–106

    Article  CAS  Google Scholar 

  • Landsberg EC (1981) Organic acid synthesis and release of hydrogen ions in response to Fe-deficiency stress of mono- and dicotyledonous plant species. J Plant Nutr 3:579–591

    CAS  Google Scholar 

  • Landsberg EC (1986) Function of rhizodermal transfer cells in the Fe stress response mechanisms of Capsicum annuum L. Plant Physiol 82:511–517

    PubMed  CAS  Google Scholar 

  • Lea PJ, Morot-Gaudry J-F (2001) Plant nitrogen. Springer-Verlag, INRA Paris, Berlin, 407 p

    Google Scholar 

  • López-Millán A-F, Morales F, Abadía A, Abadía J (2000a) Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiol 124:873–884

    Article  Google Scholar 

  • López-Millán A-F, Morales F, Andaluz S, Gogorcena Y, Abadía A, Abadía J (2000b) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol 124:885–897

    Article  Google Scholar 

  • Loulakakis KA, Roubelakis-Angelakis KA (2001) Nitrogen assimilation in grapevine. In: Roubelakis-Angelakis KA (ed) Molecular biology and biotechnology of the grapevine. Kluwer Academic Publishers, Dordrecht/Boston/London, pp 59–85

    Google Scholar 

  • Lucena JJ (2000) Effects of bicarbonate, nitrate and other environmental factors on iron deficiency chlorosis. A review. J Plant Nutr 23:1591–1606

    CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, II edn. Academic Press Limited, London, 889 p

    Google Scholar 

  • McCluskey J, Herdman L, Skene KR (2004) Iron deficiency induces changes in metabolism of citrate in lateral roots and cluster roots of Lupinus albus. Physiol Plant 121:586–594

    Article  CAS  Google Scholar 

  • Mengel K (1994) Iron availability in plant tissues – iron chlorosis in calcareous soil. Plant Soil 165:275–283

    Article  CAS  Google Scholar 

  • Mengel K, Kirkby EA (2001) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Mengel K, Malissiovas N (1982) Light-dependent proton excretion by roots of entire vine plants (Vitis vinifera L.). Z Pflanzenernaehr Bodenk 145:261–267

    Article  CAS  Google Scholar 

  • Mengel K, Planker R, Hoffmann B (1994) Relationship between leaf apoplast pH and iron chlorosis of sunflower (Helianthuus annuus L.). J Plant Nutr 17:1053–1065

    CAS  Google Scholar 

  • Moing A, Maucourt M, Renaud C, Gaudillère M, Brouquisse R, Lebouteiller B, Gousset-Dupont A, Vidal J, Granot D, Denoyes-Rothan B, Lerceteau-Köhler E, Rolin D (2004) Quantitative metabolic profiling by 1-dimensional 1H-NMR analyses: application to plant genetics and functional genomics. Funct Plant Biol 31:889–902

    Article  CAS  Google Scholar 

  • Nikolic M, Römheld V (2003) Nitrate does not result in iron inactivation in the apoplast of sunflower leaves. Plant Physiol 132:1303–1314

    Article  PubMed  CAS  Google Scholar 

  • Nikolic M, Römheld V, Merkt N (2000) Effect of bicarbonate on uptake and translocation of 59Fe in two grapevine rootstocks differing in their resistance of Fe deficiency chlorosis. Vitis 39:145–149

    CAS  Google Scholar 

  • Nisi PD, Zocchi G (2000) Phosphoenolpyruvate carboxylase in cucumber (Cucumis sativus L.) roots under iron deficiency: activity and kinetic characterization. J Exp Bot 51:1903–1909

    Article  PubMed  CAS  Google Scholar 

  • Ollat N, Laborde B, Neveux M, Diakou-Verdin P, Renaud C, Moing A (2003) Organic acid metabolism in roots of various grapevine (Vitis) rootstocks submitted to iron deficiency and bicarbonate nutrition. J Plant Nutr 26:2165–2176

    Article  CAS  Google Scholar 

  • Pasqualini S, Ederli L, Piccioni C, Batini P, Belluci M, Arcioni S, Antonielli M (2001) Metabolic regulation and gene expression of root phosphoenolpyruvate carboxylase by different nitrogen sources. Plant Cell Environ 24:

  • Rodriguez-Lovelle B, Gaudillère JP (2002) Carbon and nitrogen partitioning in either fruiting or non-fruiting grapevines: effects of nitrogen limitation before and after veraison. Aust J Grape Wine Res 8:86–94

    Google Scholar 

  • Rombolà AD, Bruggemann W, López-Millán AF, Tagliavini M, Abadía J, Marangoni B, Moog PR (2002) Biochemical responses to iron deficiency in kiwifruit (Actinidia deliciosa). Tree Physiol 22:869–875

    PubMed  Google Scholar 

  • Rombolà AD, Gogorcena Y, Larbi A, Morales F, Baldi E, Marangoni B, Tagliavini M, Abadia J (2005) Iron deficiency-induced changes in carbon fixation and leaf elemental composition of sugar beet (Beta vulgaris) plants. Plant Soil 271:39–45

    Article  CAS  Google Scholar 

  • Römheld V (1987) Different strategies for iron acquisition in higher plants. Physiol Plant 70:231–234

    Article  Google Scholar 

  • Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H+-ATPase genes differentially expressed in iron-deficient cucumber plants. Plant Physiol Biochem 43:287–292

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W (2003) Iron solutions: acquisition strategies and signalling pathways in plants. Trends Plant Sci 8:188–193

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Byrne DH, Reed DW (1993) Iron chlorosis development and growth response of peach rootstocks to bicarbonate. J Plant Nutr 16:1039–1046

    CAS  Google Scholar 

  • Smith F (1974) Malate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie/Academic Press, New York, pp 163–175

    Google Scholar 

  • Smolders AJP, Hendriks RJJ, Campschreur HM, Roelofs JGM (1997) Nitrate induced iron deficiency iron deficiency chlorosis in Juncus acutiflorus. Plant Soil 196:37–45

    Article  CAS  Google Scholar 

  • Srere PA (1967) Citrate synthase. In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic Press, New York, pp 3–11

    Google Scholar 

  • Suárez MF, Avila C, Gallardo F, Canton FR, Garcia-Gutierrez A, Claros MG, Canovas FM (2002) Molecular and enzymatic analysis of ammonium assimilation in woody plants. J Exp Bot 53:891–904

    Article  PubMed  Google Scholar 

  • Sun XP, Wang SY, Tong YA, Korcak RF, Faust M (1987) Metabolic changes in iron-deficient apple seedlings. J Plant Nutr 10:1021–1030

    CAS  Google Scholar 

  • Susin S, Abadía A, Gonzalez-Reyes JA, Lucena JJ, Abadía J (1996) The pH requirement for in vivo activity of the iron-deficiency induced “turbo” ferric chelate reductase: a comparison of the iron-deficiency-induced iron reductase activities of intact plants and isolated plasma membrane fractions in sugar beet. Plant Physiol 110:111–123

    PubMed  CAS  Google Scholar 

  • Tagliavini M, Rombolà AD (2001) Iron deficiency and chlorosis in orchard and vineyard ecosystems. Eur J Agron 15:71–92

    Article  CAS  Google Scholar 

  • Toulon V, Sentenac H, Thibaud J-B, Davidian J-C, Moulineau C, Grignon C (1992) Role of apoplast acidification by the H+ pump. Effect on the sensitivity to pH and CO2 of iron reduction by roots of Brassica napus L. Planta 186:212–218

    Article  CAS  Google Scholar 

  • Vance CP, Stade S, Maxwell CA (1983) Alfalfa root nodule carbon dioxide fixation. I: association with nitrogen fixation and incorporation into amino acids. Plant Physiol 72:469–473

    Article  PubMed  CAS  Google Scholar 

  • Varanini Z, Maggioni A (1982) Iron reduction and uptake by grapevine roots. J Plant Nut 5:521–529

    CAS  Google Scholar 

  • von Wirén N, Gojon A, Chaillou S, Raper D (2001) Mechanisms and regulation of ammonium uptake in higher plants. In: Lea PJ, Morot-Gaudry J-F (eds) Plant nitrogen. Springer-Verlag, INRA éditions, Berlin, pp 61–77

    Google Scholar 

  • Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844

    Article  PubMed  CAS  Google Scholar 

  • Zerihun A, Treeby MT (2002) Biomass distribution and nitrate assimilation in response to N supply for Vitis vinifera L. cv. Cabernet Sauvignon on five Vitis rootstock genotypes. Aust J Grape Wine Res 8:157–162

    CAS  Google Scholar 

Download references

Acknowledgments

This work was partly funded by the Franco-Spanish bilateral cooperation program (Picasso Program HF2003-273) and by Aquitaine-Aragón cooperation programs (Aq23, Aq25). Sergio Jiménez was supported by a I3P fellowship from CSIC/FSE (Consejo Superior de Investigaciones Científicas/Fondo Social Europeo) and a travel fellowship from DGA/CAI (CA 5/03). We would like to thank Catherine Deborde and Mickaël Maucourt for assistance with 1H-NMR analysis and data processing, Dr Annick Moing for critical reading of the manuscript, and Dr Tatiana Buhner for helpful English reading.

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Authors and Affiliations

  1. Departamento de Pomología, Estación Experimental de Aula Dei, CSIC, Apdo. 202, 50080, Zaragoza, Spain

    S. Jiménez & Y. Gogorcena

  2. Unité de Recherches sur les Espèces Fruitières et la Vigne, INRA, BP 81, 71 avenue Edouard Bourleaux, 33 883, Villenave d’Ornon, France

    C. Hévin & N. Ollat

  3. Dipartimento di Colture Arboree, Università di Bologna, Via G. Fanin 46, 40127, Bologna, Italy

    A. D. Rombolà

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  1. S. Jiménez
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  2. Y. Gogorcena
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  3. C. Hévin
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  4. A. D. Rombolà
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  5. N. Ollat
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Correspondence to N. Ollat.

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Jiménez, S., Gogorcena, Y., Hévin, C. et al. Nitrogen nutrition influences some biochemical responses to iron deficiency in tolerant and sensitive genotypes of Vitis . Plant Soil 290, 343–355 (2007). https://doi.org/10.1007/s11104-006-9166-4

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  • DOI: https://doi.org/10.1007/s11104-006-9166-4

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