Changes in the concentration of organic acids in roots and leaves of carob-tree under Fe deficiency
Pedro José Correia A F , Florinda Gama A , Teresa Saavedra A , Maria Graça Miguel B , José Paulo Da Silva C , Anunciación Abadía D , Amarilis de Varennes E and Maribela Pestana A
+ Author Affiliations
- Author Affiliations
A ICAAM, Universidade do Algarve, Faculdade de Ciências e Tecnologia, Campus de Gambelas, 8005-139 Faro, Portugal.
B IBB-CBV, Universidade do Algarve, Faculdade de Ciências e Tecnologia, Departamento de Química e Farmácia, Campus de Gambelas, 8005-139 Faro, Portugal.
C CIQA – Faculdade de Ciências e Tecnologia, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal.
D Estación Experimental de Aula Dei, CSIC, Departamento de Nutrición Vegetal, 50080 Zaragoza, Spain.
E CEER, Instituto Superior de Agronomia - ULisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal.
F Corresponding author. Email: pcorreia@ualg.pt
Functional Plant Biology 41(5) 496-504 https://doi.org/10.1071/FP13204
Submitted: 9 July 2013 Accepted: 1 December 2013 Published: 6 January 2014
Abstract
Several fruit trees are able to cope with iron (Fe) deficiency when grown in calcareous soils in the Mediterranean region, although information regarding well adapted slow-growing species is scarce, and the mechanisms activated by these species are not described in the literature. A crucial issue related to tolerance is the need to transport Fe over relatively long distances inside the plant. To evaluate the possible role of organic acids in the movement of Fe in tolerant plants, we studied the concentration of low molecular weight organic acids in several organs of 1-year old carob plants grown for 55 days in nutrient solutions without Fe (0 µM Fe) or with 1 µM Fe and 10 µM Fe. Roots, stems and leaves were harvested, and the biomass, Fe and organic acid contents quantified. Total leaf chlorophyll (Chl) was evaluated in young leaves over the experimental period and the activity of root ferric chelate-reductase (FC-R; EC 1.16.1.17) was determined after 35 days, when deficiency symptoms appeared. Iron chlorosis was observed only at the end of the experiment in plants grown in the absence of Fe, and these plants had a smaller DW of leaves and also significant greater activity of root FC-R. Iron deficiency (Fe0 and Fe1 treatments) induced significant changes in the concentrations of succinic, malic, citric and fumaric acids, which increased in roots, or in basal, middle and apical leaves. There were significant correlations between most organic acids (with the exceptions of 2-oxoglutaric and tartaric acids) and leaf Chl. Analysis of each type of leaf showed that more succinic and malic acids were present in young chlorotic leaves while the reverse was true for quinic acid. These changes in organic acids followed a root-to-foliage pathway that was similar in all leaf types and particularly evident in young chlorotic leaves. We hypothesised that it was associated with Fe transport from roots to aboveground tissues, as there were significant differences in Fe contents between treatments with and without Fe.
Additional keywords: Ceratonia siliqua, FC-R activity, leaf chlorophyll, vegetative growth.
References
Abadía J, Abadía A (1993) Iron and pigments. In ‘Iron chelation in plants and soil microorganisms’. (Eds LL Barton, BC Hemming) pp. 327–343. (Academic Press Inc.: San Diego, CA, USA)Abadía J, López-Millán AF, Rombolà AD, Abadía A (2002) Organic acids and Fe deficiency: a review. Plant and Soil 241, 75–86.
| Organic acids and Fe deficiency: a review.Crossref | GoogleScholarGoogle Scholar |
Abadía J, Álvarez-Fernández A, Rombolà AD, Sanz M, Tagliavini M, Abadía A (2004) Technologies for the diagnosis and remediation of Fe deficiency. Soil Science and Plant Nutrition 50, 965–971.
| Technologies for the diagnosis and remediation of Fe deficiency.Crossref | GoogleScholarGoogle Scholar |
Abadía J, Vázquez S, Rellán-Álvarez R, El-Jendoubi H, Abadía A, Álvarez-Fernández A, López-Millán AF (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiology and Biochemistry 49, 471–482.
| Towards a knowledge-based correction of iron chlorosis.Crossref | GoogleScholarGoogle Scholar | 21349731PubMed |
Alhendawi RA, Römheld V, Kirkby EA, Marschner H (1997) Influence of increasing bicarbonate concentrations on plant growth, organic acid accumulation in roots and iron uptake by barley, sorghum, and maize. Journal of Plant Nutrition 20, 1731–1753.
| Influence of increasing bicarbonate concentrations on plant growth, organic acid accumulation in roots and iron uptake by barley, sorghum, and maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsFyltL8%3D&md5=9d4fbf32ff8929893c680118437edcffCAS |
AOAC (1990) ‘Official methods of analysis.’ (Association of Official Agricultural Chemists: Washington, DC, USA)
Bienfait HF, Bino RJ, Van der Blick AM, Duivenvoorden JF, Fontaine JM (1983) Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris. Physiologia Plantarum 59, 196–202.
| Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvFerurk%3D&md5=f9bc425ecf9efc7637e41c3495802644CAS |
Correia PJ, Martins-Loução MA (2005) The use of macronutrients and water in marginal Mediterranean areas: the case of carob-tree. Field Crops Research 91, 1–6.
| The use of macronutrients and water in marginal Mediterranean areas: the case of carob-tree.Crossref | GoogleScholarGoogle Scholar |
Correia PJ, Anastácio I, Candeias MF, Martins-Loução MA (2002) Nutritional diagnosis in carob-tree (Ceratonia siliqua L.): relationships between yield and leaf mineral concentration. Crop Science 42, 1577–1583.
| Nutritional diagnosis in carob-tree (Ceratonia siliqua L.): relationships between yield and leaf mineral concentration.Crossref | GoogleScholarGoogle Scholar |
Correia PJ, Pestana M, Martins-Loução MA (2003) Nutrient deficiencies in carob (Ceratonia siliqua L.) grown in solution culture. Journal of Horticultural Science & Biotechnology 78, 847–852.
Correia PJ, Pestana M, Domingos I, Martins-Loução MA (2008) Nutritional evaluation of nitrogen and potassium fertilization of carob tree under dry-farming conditions. Communications in Soil Science and Plant Analysis 39, 652–666.
| Nutritional evaluation of nitrogen and potassium fertilization of carob tree under dry-farming conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1Cls7o%3D&md5=f5448321387aa34c1ecae7c8ee9a17cfCAS |
Donnini S, Castagna A, Ranieri A, Zocchi G (2009) Differential responses in pear and quince genotypes induced by Fe deficiency and bicarbonate. Journal of Plant Physiology 166, 1181–1193.
| Differential responses in pear and quince genotypes induced by Fe deficiency and bicarbonate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFelsLs%3D&md5=6ce07df6992fae0981d0fb914dfeac49CAS | 19269060PubMed |
Donnini S, De Nisi P, Gabatolli D, Tato L, Zocchi G (2012) Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability. Plant, Cell & Environment 35, 1171–1184.
| Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptF2ktbo%3D&md5=e98c5f6214858a2baf2a2f0338e7e07fCAS |
Gogorcena Y, Abadía J, Abadía A (2005) New technique for screening iron-efficient genotypes in peach rootstocks: elicitation of root ferric chelate reductase by manipulation of external iron concentrations. Journal of Plant Nutrition 27, 1701–1715.
| New technique for screening iron-efficient genotypes in peach rootstocks: elicitation of root ferric chelate reductase by manipulation of external iron concentrations.Crossref | GoogleScholarGoogle Scholar |
Jiménez S, Morales F, Abadía A, Abadía J, Moreno MA, Gogorcena Y (2009) Elemental 2-D mapping and changes in leaf iron and chlorophyll in response to iron re-supply in iron-deficient GF 677 peach-almond hybrid. Plant and Soil 315, 93–106.
| Elemental 2-D mapping and changes in leaf iron and chlorophyll in response to iron re-supply in iron-deficient GF 677 peach-almond hybrid.Crossref | GoogleScholarGoogle Scholar |
Jiménez S, Ollat N, Deborde C, Maucourt M, Rellán-Álvarez R, Moreno M, Gogorcena Y (2011) Metabolic response in roots of Prunus rootstocks submitted to iron chlorosis. Journal of Plant Physiology 168, 415–423.
| Metabolic response in roots of Prunus rootstocks submitted to iron chlorosis.Crossref | GoogleScholarGoogle Scholar | 20952094PubMed |
Larbi A, Morales F, Abadía J, Abadía A (2003) Effects of branch solid Fe sulphate implants on xylem sap composition in field-grown peach and pear: changes in Fe, organic anions and pH. Journal of Plant Physiology 160, 1473–1481.
| Effects of branch solid Fe sulphate implants on xylem sap composition in field-grown peach and pear: changes in Fe, organic anions and pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFKlurc%3D&md5=c35de7e78fc4d254ff22c3e398d9bf36CAS | 14717440PubMed |
Larbi A, Morales F, Abadía A, Abadía J (2010) Changes in iron and organic acid concentrations in xylem sap and apoplastic fluid of iron-deficient Beta vulgaris plants in response to iron resupply. Journal of Plant Physiology 167, 255–260.
| Changes in iron and organic acid concentrations in xylem sap and apoplastic fluid of iron-deficient Beta vulgaris plants in response to iron resupply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFOnsbs%3D&md5=4b06db41f38605fc899e01b4ad9ad65aCAS | 19854536PubMed |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Llosá MJ, Bermejo A, Cano A, Quiñones A, Forner-Giner MA (2009) The citrus rootstocks Cleopatra mandarin, Poncirus trifoliata, Forner-Alcaide 5 and Forner-Alcaide 13 vary in susceptibility to iron deficiency chlorosis. Journal of the American Pomological Science 63, 160–167.
López-Millán AF, Morales F, Abadía A, Abadía J (2001a) Iron deficiency-associated changes in the composition of the leaf apoplastic fluid from field-grown pear (Pyrus communis L.) trees. Journal of Experimental Botany 52, 1489–1498.
| Iron deficiency-associated changes in the composition of the leaf apoplastic fluid from field-grown pear (Pyrus communis L.) trees.Crossref | GoogleScholarGoogle Scholar | 11457909PubMed |
López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J (2001b) Iron-resupply mediated deactivation of Fe-deficiency stress responses in roots of sugar beet. Australian Journal of Plant Physiology 28, 171–180.
López-Millán A, Morales F, Gogorcena Y, Abadía A, Abadía J (2009) Metabolic responses in iron deficient tomato plants. Journal of Plant Physiology 166, 375–384.
| Metabolic responses in iron deficient tomato plants.Crossref | GoogleScholarGoogle Scholar | 18760500PubMed |
López-Millán A, Grusak MA, Abadía J (2012) Carboxylate metabolism changes induced by Fe deficiency in barley, a Strategy II plant species. Journal of Plant Physiology 169, 1121–1124.
| Carboxylate metabolism changes induced by Fe deficiency in barley, a Strategy II plant species.Crossref | GoogleScholarGoogle Scholar | 22709961PubMed |
Martínez-Cuenca MR, Iglesias DJ, Talón M, Abadía J, López-Millán A, Primo-Millo E, Legaz F (2013) Metabolic responses to iron deficiency in roots of Carrizo citrange (Citrus sinensis (L.) Osbeck.× Poncirus trifoliata (L.) Raf.). Tree Physiology 33, 320–329.
| Metabolic responses to iron deficiency in roots of Carrizo citrange (Citrus sinensis (L.) Osbeck.× Poncirus trifoliata (L.) Raf.).Crossref | GoogleScholarGoogle Scholar | 23462311PubMed |
Ollat N, Labordea B, Neveuxa M, Verdinc PD, Renauda C, Moingab A (2003) Organic acid metabolism in roots of various grapevine (Vitis) rootstocks submitted to iron deficiency and bicarbonate nutrition. Journal of Plant Nutrition 26, 2165–2176.
| Organic acid metabolism in roots of various grapevine (Vitis) rootstocks submitted to iron deficiency and bicarbonate nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFCgtbc%3D&md5=50378664541fc04af2cfdb887da5359bCAS |
Pestana M, de Varennes A, Faria EA (2004) Lime-induced iron chlorosis in fruit trees. In ‘Production practices and quality assessment of food crops. Vol. 2: Plant mineral nutrition and pesticide management’. (Eds R Dris, SM Jain) pp. 171–215. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Pestana M, Gama F, Saavedra T, de Varennes A, Correia PJ (2012) The root ferric-chelate reductase of Ceratonia siliqua (L.) and Poncirus trifoliata (L.) Raf. respond differently to levels of iron. Scientia Horticulturae 135, 65–67.
| The root ferric-chelate reductase of Ceratonia siliqua (L.) and Poncirus trifoliata (L.) Raf. respond differently to levels of iron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFaltrw%3D&md5=403c7c12de077e79e8d4a33576e4ae1dCAS |
Rellán-Álvarez R, Giner-Martínez-Sierra J, Orduna J, Orera I, Rodríguez-Castrillón JA, García-Alonso JI, Abadía J, Álvarez-Fernández A (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant & Cell Physiology 51, 91–102.
| Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport.Crossref | GoogleScholarGoogle Scholar |
Rellán-Álvarez R, López-Gomollón S, Abadía J, Álvarez-Fernández A (2011) Development of a new HPLC-ESI-TOFMS method for the determination of low molecular mass organic acids in plant tissue extracts. Journal of Agricultural and Food Chemistry 59, 6864–6870.
| Development of a new HPLC-ESI-TOFMS method for the determination of low molecular mass organic acids in plant tissue extracts.Crossref | GoogleScholarGoogle Scholar | 21619056PubMed |
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 Physiology 22, 869–875.
| Biochemical responses to iron deficiency in kiwifruit (Actinidia deliciosa).Crossref | GoogleScholarGoogle Scholar | 12184976PubMed |
Romera FJ, Alcántara E (2004) Ethylene involvement in the regulation of Fe-deficiency stress responses by Strategy I plants. Functional Plant Biology 31, 315–328.
| Ethylene involvement in the regulation of Fe-deficiency stress responses by Strategy I plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs12murs%3D&md5=9d592760c8e93a4671b85a936a46a632CAS |
Römheld V, Marschner H (1986) Mobilization of iron in the rizosphere of different plant species. Advances in Plant Nutrition 2, 155–204.
