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Organic acids metabolism in roots of grapevine rootstocks under severe iron deficiency

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Abstract

Background and aims

In many important viticultural areas of the Mediterranean basin, plants often face prolonged periods of scarce iron (Fe) availability in the soil. The objective of the present work was to perform a comparative analysis of physiological and biochemical responses of Vitis genotypes to severe Fe deficiency.

Methods

Three grapevine rootstocks differing in susceptibility to Fe chlorosis were grown with and without Fe in the nutrient solution.

Results

Rootstock 101-14, susceptible to Fe chlorosis, responded to severe Fe deficiency by reducing the root activity of phosphoenolpyruvate carboxylase (PEPC) and malate dehydrogenase (MDH), however, it accumulated high levels of citric acid. By contrast, rootstock 110 Richter, tolerant to Fe chlorosis, maintained an active metabolism of organic acids, but citric acid accumulation was lower than in 101-14. Similarly to 101-14, rootstock SO4 showed a strong decrease in PEPC and MDH activities. Nevertheless it maintained moderate citric acid levels in the roots, mimicking the response by 110 Richter.

Conclusions

Root PEPC and MDH activities can be used as tools for screening Fe chlorosis tolerance. Conversely, organic acids accumulation in roots may not be a reliable indicator of Fe chlorosis tolerance, particularly under conditions of severe Fe deficiency, because of their probable exudation by roots. Our results show that drawing sound conclusions from screening programs involving Fe deficiency tolerance requires short as well as long-term assessment of responses to Fe deprivation.

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Abbreviations

BSA:

Bovine serum albumin

CoA:

Coenzyme A

CS:

Citrate synthase

DW:

Dry weight

EDTA:

Ethylenediaminetetraacetic acid

FW:

Fresh weight

MDH:

Malate dehydrogenase

NADP+-IDH:

Isocitrate dehydrogenase

PEPC:

Phosphoenolpyruvate carboxylase

TCA:

Tricarboxylic acid

References

  • Bavaresco LE, Giachino E, Pezzutto S (2003) Grapevine rootstock effects on lime-induced chlorosis, nutrient uptake, and source-sink relationships. J Plant Nutr 26:1451–1465

    Article  CAS  Google Scholar 

  • Bavaresco L, van Zeller MI, Civardi S, Gatti M, Ferrari F (2010) Effects of traditional and new methods on overcoming lime-induced chlorosis of grapevine. Am J Enol Vitic 61:186–190

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  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 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25

    Article  CAS  Google Scholar 

  • Chollet R, Vidal J, O’Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47:273–298

    Article  CAS  PubMed  Google Scholar 

  • Covarrubias JI, Rombolà AD (2013) Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate. Plant Soil 370:305–315

    Article  CAS  Google Scholar 

  • Covarrubias JI, Pisi A, Rombolà AD (2014) Evaluation of sustainable management techniques for preventing iron chlorosis in the grapevine. Aust J Grape Wine Res 20:149–159

    Article  CAS  Google Scholar 

  • De Nisi P, Zocchi G (2000) Phosphoenolpyruvate carboxylase in cucumber (Cucumis sativus L.) roots under iron deficiency: activity and kinetic characterization. J Exp Bot 51(352):1903–1909

    Article  CAS  PubMed  Google Scholar 

  • De Nisi P, Vigani G, Zocchi G (2010) Modulation of iron responsive gene expression and enzymatic activities in response to changes of the iron nutritional status in Cucumis sativus L. Available from Nature Precedings. doi:10.1038/npre.2010.4658.1

  • Donnini S, Castagna A, Ranieri A, Zocchi G (2009) Differential responses in pear and quince genotypes induced by Fe deficiency and bicarbonate. J Plant Physiol 166:1181–1193

    Article  CAS  PubMed  Google Scholar 

  • Donnini S, Prinsi B, Negri AS, Vigani G, Espen L, Zocchi G (2010) Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots. BMC Plant Biol 10:268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G, Hodges M (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62(4):1467–1482

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Jelali N, Wissal M, Dell’Orto M, Abdellya C, Gharsalli M, Zocchi G (2010) Changes of metabolic responses to direct and induced Fe deficiency of two Pisum sativum cultivars. Environ Exp Bot 68:238–246

    Article  CAS  Google Scholar 

  • Jimenez S, Gogorcena Y, Hévin C, Rombolà AD, Ollat N (2007) Nitrogen nutrition influences some biochemical responses to iron deficiency in tolerant and sensitive genotypes of Vitis. Plant Soil 290:343–355

    Article  CAS  Google Scholar 

  • Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280

    Article  CAS  PubMed  Google Scholar 

  • Lance C, Rustin P (1984) The central role of malate in plant metabolism. Physiol Veg 22(5):625–641

    CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166:375–384

    Article  PubMed  Google Scholar 

  • López-Rayo S, Di Foggia M, Bombai G, Yunta F, Rodrigues-Moreira E, Filippini G, Pisi A, Rombolà AD (2014) Blood-derived compounds can efficiently prevent iron deficiency in grapevine. Aust J Grape Wine Res 21:135–142

    Article  Google Scholar 

  • Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518

    Article  CAS  PubMed  Google Scholar 

  • Neumann G (2006) Root exudates and organic composition of plant roots. In: Luster J, Finlay R (eds) Handbook of methods used in rhizosphere research. Swiss Federal Research Institute WSL, Birmensdorf, 536 p

    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 to Fe deficiency chlorosis. Vitis 39(4):145–149

    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(10&11):2165–2176

    Article  CAS  Google Scholar 

  • Rodríguez-Celma J, Lattanzio G, Grusak MA, Abadía A, Abadía J, López-Millán AF (2011) Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin biosynthesis. J Proteome Res 10:2590–2601

    Article  PubMed  Google Scholar 

  • Rombolà AD, Tagliavini M (2006) Iron nutrition of fruit tree crops. In: Abadía J, Barton L (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Berlin, pp 61–83

    Chapter  Google Scholar 

  • Rombolà AD, Brüggemann 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

    Article  PubMed  Google Scholar 

  • Römheld V, Marschner H (1986) Mobilitation of iron in the rhizosphere of different plant species. Adv Plant Nutr 2:123–218

    Google Scholar 

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

    Google Scholar 

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

    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 

  • Tagliavini M, Rombolà AD, Marangoni B (1995) Response to Fe-deficiency stress of pear and quince genotypes. J Plant Nutr 18(11):2465–2482

    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 Central  CAS  PubMed  Google Scholar 

  • Wong KF, Davies DD (1973) Regulation of phosphoenolpyruvate carboxylase of Zea mays by metabolites. Biochem J 131:451–458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yunta F, Di Foggia M, Bellido-Díaz V, Morales-Calderón M, Tessarin P, López-Rayo S, Tinti A, Kovács K, Klencsár Z, Fodor F, Rombolà AD (2013) Blood meal-based compound. Good choice as iron fertilizer for organic farming. J Agric Food Chem 61:3995–4003

    Article  CAS  PubMed  Google Scholar 

  • Zocchi G (2006) Metabolic changes in iron-stressed dicotyledonous plants. In: Abadía J, Barton L (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Berlin, pp 359–370

    Chapter  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of Chile and the Erasmus Mundus External Cooperation Window for Chile (Lot 17)-European Union Community for Doctoral Scholarships to José Ignacio Covarrubias.

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Authors and Affiliations

  1. Facultad de Ciencias Agronómicas, Universidad de Chile, Av. Santa Rosa, 11315, Santiago, Chile

    José Ignacio Covarrubias

  2. Department of Agricultural Sciences, University of Bologna, Viale G. Fanin 44, 40127, Bologna, Italy

    Adamo Domenico Rombolà

Authors
  1. José Ignacio Covarrubias
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  2. Adamo Domenico Rombolà
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Correspondence to Adamo Domenico Rombolà.

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Responsible Editor: Yong Chao Liang.

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Covarrubias, J.I., Rombolà, A.D. Organic acids metabolism in roots of grapevine rootstocks under severe iron deficiency. Plant Soil 394, 165–175 (2015). https://doi.org/10.1007/s11104-015-2530-5

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