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Published online 20 September 2006
Published in Soil Sci Soc Am J 70:1945-1950 (2006)
DOI: 10.2136/sssaj2005.0343
© 2006 Soil Science Society of America
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Nutrient Management & Soil & Plant Analysis

Predicting Iron Chlorosis of Lupin in Calcareous Spanish Soils from Iron Extracts

Ana de Santiago and Antonio Delgado*

Dpto. Ciencias Agroforestales, EUITA, Univ. de Sevilla, Ctra. Utrera km 1, 41013 Seville, Spain

* Corresponding author (adelgado{at}us.es)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Iron deficiency chlorosis is a major nutritional problem affecting sensitive cultivated plants in calcareous soils. Our main objective was to study the suitability of various Fe extracts for predicting the incidence of Fe deficiency chlorosis in calcareous soils from southern Spain. Six single Fe extractions were used: unbuffered hydroxylamine (room temperature), DTPA (diethylenetriaminepentaacetic acid) at 2 and 17 h, "rapid" ammonium oxalate, ammonium oxalate, and pyrophosphate. The Fe forms that account for most of the Fe supplied to plants were studied by using a sequential Fe fractionation process involving four extractants: citrate–bicarbonate, citrate at pH 6, citrate–ascorbate (a mild reductant), and citrate–bicarbonate–dithionite (a strong reductant). Suitability of Fe extracts for predicting Fe chlorosis was checked by establishing correlations between the amount of Fe extracted from soil and the chlorophyll content in white lupin (Lupinus albus L.). The amounts of Fe extracted by hydroxylamine accounted for a minimal portion of Fe associated with oxides, thus indicating that this extractant is not efficient at reducing Fe oxides. Hydroxylamine Fe, however, accounted for 63 and 72% of the variance in chlorophyll meter readings at 2 and 3 wk of growth, respectively, in contrast to "rapid" oxalate (32 and 11%) and DTPA at 2 h (29 and 15%). At 3 wk of growth, the variance in meter readings explained by hydroxylamine Fe was much higher than that explained by the active CaCO3 equivalent (56%). This ability of hydroxylamine Fe to predict chlorophyll meter readings is due to the relationship of the Fe extract to poorly crystalline Fe fractions, which showed the strongest relationship with the active CaCO3 content (R2 = 0.84, P < 0.001).

Abbreviations: ACCE, "active" calcium carbonate equivalent • C, citrate • CA, citrate–ascorbate • CB, citrate–bicarbonate • CBD, citrate–bicarbonate–dithionite • DTPA, diethylenetriaminepentaacetic acid


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
IRON deficiency chlorosis is a major nutritional problem affecting cultivated plants in calcareous soils, characterized by yellowing of young leaves that contrast with the green color frequently observed in the more mature leaves. Cultivated plants differ in their susceptibility to Fe deficiency depending on their mechanisms of Fe acquisition, particularly in their ability to release Fe-chelating compounds (Römheld and Marschner, 1986; Ma and Nomoto, 1996; Ma et al., 2003). In sensitive plants, severe Fe deficiency results in high economic losses, particularly in perennial crops (Tagliavini and Rombolà, 2001; Gruber and Kosegarten, 2002).

The low availability of Fe in calcareous soils can be ascribed to (i) an extremely low solubility of soil Fe, which is essentially in ferric oxide form (Miller et al., 1984; Mengel, 1994), and (ii) reduced Fe uptake from the apoplast into the symplast, which can be related to the pH of the former (Brand et al., 2000a; Yu et al., 2000), influenced by a high bicarbonate concentration in calcareous soils (Mengel, 1994; Lucena, 2000). The effect of the apoplastic pH and its relationship with soil bicarbonate remains unclear, however (Kosegarten et al., 1999; Nikolic and Römheld, 2002).

Although Fe chlorosis has traditionally been related to the carbonate content of soil, other properties such as the types of Fe oxide present and their content, organic matter, water content, redox potential, carbonate mineralogy, and nutrient competition may also influence Fe availability to plants (Loeppert et al., 1984; del Campillo and Torrent, 1992a; Velázquez et al., 2004). The contents of poorly crystalline Fe oxides and silicate clays seem to be particularly important in relation to the occurrence of this problem in various plant species in Mediterreanean areas (Yanguas et al., 1997; Benítez et al., 2002). Among Fe oxides, ferrihydrite, a poorly crystalline Fe oxide, has a significant influence on the supply of Fe to plants grown on calcareous soils (Loeppert and Hallmark, 1985; Morris et al., 1990); this accounts for the frequently observed relationship between the chlorophyll content and oxalate-extractable Fe (del Campillo and Torrent, 1992b). A modification of the classical ammonium oxalate Fe extraction method by Schwertmann (1964) has proved effective for the determination of "active Fe oxide forms" that account for Fe availability in calcareous soils (del Campillo and Torrent, 1992b; Benítez et al., 2002). Oxalate, however, is not such a selective extractant for Fe in poorly crystalline Fe oxides as are compounds such as citrate or ascorbate (Reyes and Torrent, 1997; Ruiz et al., 1997). Alternative extractants based on Fe chelation, such as DTPA, have often been used to estimate the active Fe pool (Lindsay and Norvell, 1978).

The primary purpose of this work was to study the suitability of various Fe extracts for predicting the incidence of Fe deficiency chlorosis in soils from southern Spain. To this end, we identified the methods that provided the best correlations between the amount of Fe extracted from soil and the chlorophyll content in white lupin.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
We examined 21 soils from the Guadalquivir Valley (southern Spain). The soils were selected in such a way as to include the most typical for Mediterranean areas according to the Soil Taxonomy (Soil Survey Staff, 1998) and span a wide range of soil properties (particularly the Fe content and "active" CaCO3 equivalent). Samples were collected from the Ap horizon (0–30 cm), air dried, and ground to pass through a 2-mm sieve before analysis.

Particle size analyses were performed by using the hydrometer method (Gee and Bauder, 1986). Organic matter was determined by dichromate oxidation (Walkley and Black, 1934), and the cation exchange capacity by using 1 M NH4OAc buffered at pH 7 (Sumner and Miller, 1996). The total CCE (CaCO3 equivalent) was determined from the weight loss on treatment with 6 M HCl (van Wesemael, 1955) and the ACCE ("active" CaCO3 equivalent) according to Drouineau (1942). The electrical conductivity and pH were measured in water (saturation extract and 1:2.5 soil/water ratio, respectively).

Six single Fe extractions were performed:

(i) unbuffered 0.5 M hydroxylammonium chloride at 298 K for 17 h (hydroxylamine) using a soil/extractant ratio of 1:20
(ii) DTPA according to Lindsay and Norvell (1978) at 2 and 17 h, which has been usually considered as an Fe availability index (at 2 h, Sims, 2000)
(iii) "rapid" ammonium oxalate extraction according to Benítez et al. (2002), which has been considered a useful Fe availability index in calcareous soils (del Campillo and Torrent, 1992b)
(iv) unbuffered ammonium oxalate to determine the amount of Fe in poorly crystalline Fe oxides (Schwertmann, 1964)
(v) pyrophosphate (Loeppert and Inskeep, 1996) to estimate the amount of Fe associated with organic matter.

A sequential Fe fractionation was performed, adapting the method of Ruiz et al. (1997) for P. This fractionation method involves four extracts:

(i) 0.27 M sodium citrate + 0.11 M NaHCO3 (CB)
(ii) 0.25 M sodium citrate at pH 6 and then 0.2 M sodium citrate at pH 6 (C)
(iii) 0.2 M sodium citrate + 0.05 M ascorbate at pH 6 (CA)
(iv) 0.27 M sodium citrate + 0.11 M NaHCO3 + 2% sodium dithionite (CBD)

Extractions were performed at 298 K and a soil/extractant ratio of 1:40. The extraction time was 17 h except in the second extraction with citrate in step (ii), which lasted 6 h. Some CB Fe and a portion of citrate-extractable Fe (the combination of the two consecutive extractions, C Fe) must correspond to Fe occluded in carbonates or complexed by organic matter. According to Reyes and Torrent (1997) and Ruiz et al. (1997), most Fe associated with poorly crystalline Fe oxides is extracted by CA. Crystalline Fe oxides not dissolved in these steps can be dissolved by using a stronger reductant (sodium dithionite) in the last step. The combined amount of Fe extracted in the four extracts can be assumed to correspond to Fe in oxides; however, it must also include some Fe associated with carbonates and organic compounds, particularly in the first few steps (Ruiz et al., 1997).

All Fe extractions were performed in triplicate using polypropylene flasks. After extraction, all the suspensions were centrifuged at 1000 g for 15 min and the supernatant was passed through a 0.22-µm pore size membrane filter. Iron in the extracts was determined by atomic absorption spectrometry.

White lupin has been described as an Fe chlorosis sensitive plant in calcareous soils (White and Robson, 1989), with significant yield reductions when it is grown in soil of pH >7.2 (Kerley and Huyghe, 2001). This plant was used to establish correlations between chlorophyll content in leaves and soil properties, in particular Fe in the different extracts. To this end, lupin was grown in quadruplicate in 350-mL pots (5.5-cm-diameter, 15-cm-high polystyrene cylinders) containing 320 g of each soil. Previously, seeds were sown in perlite irrigated with deionized water and after 14 to 15 d (four true leaves stage), the lupin plants were planted in soil (one plant per pot) and grown for 21 additional days. No chlorosis symptoms were observed at planting. The experiment was conducted in a growing chamber with a photoperiod of 12 h, a 27–23°C day–night temperature, 60% relative humidity, and a 22 W m–2 light intensity. Pots were irrigated every 2 d with a Hoagland type nutrient solution containing no Fe, and having the following composition: MgSO4 (4 mmol L–1), Ca(NO3)2 (5 mmol L–1), KNO3 (5 mmol L–1), KH2PO4 (2 mmol L–1), H3BO3 (0.092 mmol L–1), MnCl2 (0.018 mmol L–1), CuSO4 (0.0016 mmol L–1), ZnSO4 (0.0025 mmol L–1), and H2MoO4 (0.0023 mmol L–1). This nutrient supply (as a nutrient solution without Fe) has been widely used for Fe availability studies in calcareous soils (del Campillo and Torrent, 1992b; Brand et al., 2000a; Velázquez et al., 2004) to avoid the effects of other nutrient deficiencies on chlorophyll content and plant development. At 14 and 21 d after planting, chlorophyll was measured with a Minolta SPAD-502 chlorophyll meter (Minolta Camera Co., Osaka, Japan). Previously, accurate correlation between SPAD units and the chlorophyll content in L. albus leaves was checked (chlorophyll = 0.2 exp(0.04 SPAD), R2 = 0.88, P < 0.001, n = 30). Chlorophyll measurements were done in triplicate on the youngest, completely expanded leaf.

After harvest, shoots and roots of each plant were separated and dry weight determined after drying plant material at 343 K for 48 h in a forced-air oven. For Fe analysis, dried plant material (youngest expanded leaf) was ground to pass a 1-mm sieve. Then an aliquot of 0.5 g was digested with HNO3 in Teflon containers in a microwave oven (Milestone, provided by Gomensoro, Madrid, Spain), according to the manufacturer instructions. Iron contents in diluted digests were determined by atomic absorption spectrometry.

Statistical analyses involved correlations and regressions, and were done by using Statgraphics Plus 5.1 (StatPoint, 2000). Nonlinear regressions were fitted following the Marquardt procedure.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Soil properties ranged widely in studied soils (particularly CCE and ACCE, Table 1). So did Fe related to Fe oxides, viz. the combined Fe fractions according to Ruiz et al. (1997), and the different Fe fractions provided by this fractionation scheme (Table 2).


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  		Table 1. General properties of the soils from the Guadalquivir Valley (southern Spain) used to evaluate Fe extraction procedures{dagger}.

 

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  		Table 2. Extractable Fe from 21 soils from the Guadalquivir Valley (southern Spain) using different methods{dagger}.

 
"Hot" hydroxylamine extraction in acid media has proved effective at dissolving Fe oxides (McAlister and Smith, 1999; Turner, 2000). The amounts extracted in our experiment, however, account for a minimal portion of Fe associated with oxides (Table 2), thus indicating that unbuffered hydroxylamine at room temperature is not efficient at reducing Fe oxides. The amounts extracted by hydroxylamine were smaller than those obtained by using the rapid oxalate, oxalate, and pyrophosphate methods but greater than DTPA-extractable Fe (Table 2). The relationships between Fe released in single extractions and Fe fractions according to the sequential scheme (Table 3) can provide information about the sources of Fe extracted, contributing to an explanation of the potential suitability of single extractions for predicting the incidence of Fe chlorosis.


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  		Table 3. Correlation coefficients between extractable Fe{dagger} in 21 soils from the Guadalquivir Valley (southern Spain).

 
The classical extraction using ammonium oxalate (Schwertmann, 1964) provided results that were significantly correlated with CA Fe (Table 3); the latter can be assumed to be a more selective method for Fe in poorly crystalline Fe oxides (Reyes and Torrent, 1997), a fraction that accounts for 80% of oxalate-extractable Fe. As can be inferred from the correlation between oxalate-extractable Fe and the clay content of the soil (r = 0.47, P < 0.05), some Fe may be released from clay minerals by oxalate. The amount of oxalate-extractable Fe was also significantly correlated with the combination of Fe extracted by CB and C (Table 3); this can be ascribed to the oxalate extractant dissolving not only Fe in poorly crystalline oxides, but also Fe isomorphically substituting for Ca in carbonates or small particles of ferrihydrite occluded in the coarse carbonate crystals (del Campillo and Torrent, 1992b). The amounts of oxalate-extractable Fe and CA Fe were highly correlated with CBD Fe and the combined Fe fractions (Table 3). This reveals, more than an unlikely dissolution of crystalline Fe oxides by these extractants (Reyes and Torrent, 1997), that Fe associated with poorly crystalline Fe oxides accounts for an approximately fixed fraction of total Fe in oxides in these soils.

The origin of Fe extracted by pyrophosphate is unclear; besides Fe bound to organic matter, significant amounts of Fe associated with microcrystalline Fe oxide particles seem to be released by this extractant that cannot be completely removed by centrifugation (Loeppert and Inskeep, 1996), as revealed by the significant correlations observed between pyrophosphate Fe and CA Fe (r = 0.74, P < 0.001), and oxalate Fe (r = 0.69, P < 0.001; Table 3).

The amounts of Fe extracted with the rapid oxalate method were correlated with pyrophosphate-extractable Fe, CB Fe + C Fe, CA Fe, and CBD Fe (Table 3), thus indicating that the rapid oxalate extraction does not extract Fe from a single source. In some soils, rapid oxalate extracted more Fe than the classical oxalate extraction according to Schwertmann (1964; Table 2). This can be ascribed to a buffered pH in the former extraction, which may increase the efficiency of oxalate reducing Fe oxides in highly calcareous media. Iron extracted by rapid oxalate was more correlated with Fe forms related to carbonates (CB- and C-extractable Fe) than the classical one (Table 3), perhaps indicating that the buffered extraction is more effective in removing these forms of Fe as a result of an increased carbonate dissolution. On the other hand, DTPA extraction according to Lindsay and Norvell (1978, extraction at 2 h) provided values that were only significantly correlated with CB Fe + C Fe. Only when the DTPA extraction was performed at 17 h were significant correlations with oxalate-, CB+C-, and CA-extractable Fe (Table 3). The hydroxylamine extracts only exhibited significant correlations with pyrophosphate Fe and CA Fe (Table 3), which indicates that hydroxylamine-extractable Fe was more specifically related to poorly crystalline Fe oxides than other single extractions.

The amounts of Fe extracted with hydroxylamine, rapid oxalate, and DTPA (2 and 17 h) were inversely related to the ACCE (Table 4), which has traditionally been accepted as an estimator of Fe chlorosis in calcareous soils. This can be ascribed to the negative correlation between poorly crystalline Fe oxides and ACCE (r = – 0.57, P < 0.05, between CA Fe and ACCE) and to the decreased amounts of Fe extracted by reductants at a high extractant pH (Reyes and Torrent, 1997). The strongest inverse relationship between ACCE and extracted Fe was that for hydroxylamine Fe (R2 = 0.84, P < 0.001). Thus, hydroxylamine was the Fe extraction method more sensitive to the pH-buffering capacity of soil.


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  		Table 4. Best regressions predicting extractable Fe using some extractants as a function of the "active" CaCO3 equivalent in 21 soils from the Guadalquivir Valley, southern Spain.

 
Chlorophyll meter readings ranged widely (Table 5), especially after 3 wk of growth when some plants showed severe chlorosis symptoms. Dry matter production was significantly correlated with the chlorophyll content measured using SPAD after 3 wk of growth (r = 0.65, P < 0.01). The only soil properties to which dry matter production was significantly related were ACCE (Y = (0.6 + 0.04 X)–1, R2 = 0.4, P < 0.01) and hydroxylamine Fe (Y = 6 + 6 log X, R2 = 0.51, P < 0.01). Iron content in the youngest expanded leaves ranged from 26 to 101 mg kg–1 (Table 5), similar to those observed in previous studies (Sas et al., 2002), and was correlated with pyrophosphate Fe (r = 0.58, P < 0.05), CA Fe (r = 0.50, P < 0.05), and CBD Fe (r = 0.59, P < 0.05), thus indicating that Fe in the plants was not related to a specific Fe form in the soil. In agreement with previous studies (Kerley, 2000), SPAD data and dry matter production were not significantly related to the Fe content of the plants.


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  		Table 5. Chlorophyll content (SPAD) units in the last completely expanded white lupin leaf and Fe content in leaves and dry matter production at the end of the experiment.

 
In agreement with previous findings (Loeppert and Hallmark, 1985; Morris et al., 1990; del Campillo and Torrent, 1992b), the Fe fraction associated with poorly crystalline Fe oxides was the only one related to the chlorophyll meter readings (CA Fe, according to Ruiz et al., 1997). Citrate–ascorbate-extractable Fe was more closely related to SPAD data than oxalate Fe; this can be ascribed to more selective dissolution of poorly crystalline oxides by citrate–ascorbate than by oxalate (Reyes and Torrent, 1997). Iron extracted in previous steps of the Ruiz et al. (1997) scheme (CB and C) was unrelated to the chlorophyll meter readings (Table 6); although these fractions must include some Fe from poorly crystalline Fe oxides, significant amounts of low-availability Fe forms (Fe and ferrihydrite occluded in carbonate particles) must also be extracted.


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  		Table 6. Regressions predicting the chlorophyll content (SPAD units) in the last completely expanded leaf of white lupin after 2 and 3 wk of growth in soils from the Guadalquivir Valley, southern Spain.

 
Hydroxylamine Fe accounted for 63 and 72% of the variance in chlorophyll meter readings at 2 and 3 wk of growth (Table 6), respectively. This is in contrast with the low variance explained by rapid oxalate (32 and 11%) and the classical DTPA extraction at 2 h (Table 6). The amount of Fe extracted by DTPA at 17 h was only significantly related to the chlorophyll meter readings after 2 wk of growth (R2 = 0.41, P < 0.01).

Hydroxylamine-extractable Fe and ACCE provided the best estimates of the chlorophyll content measured using SPAD after 2 and 3 wk of growth (Table 6); after 3 wk, hydroxylamine Fe was clearly the best predictive index for chlorophyll meter readings (Table 6). The predictive value of ACCE can be ascribed to the fact that bicarbonate in the soil solution is a key factor explaining lupin tolerance to Fe chlorosis. Römheld (1986) found Fe chlorosis in lupins to be due to a decreased efficiency of the roots to solubilize Fe in a pH-buffered medium, and Brand et al. (2000b) suggested that HCO3– inhibits Fe uptake. This is consistent with the finding of Dinkelaker et al. (1989) that Fe availability in white lupin is related to strong acidification of the rhizosphere through the release of acids (mainly citrate) by roots. Citrate in acid media promotes Fe3+ reduction and increases Fe availability as a result (Marschner et al., 1987); however, Fe3+ reduction by citrate is decreased above pH 6 (Reyes and Torrent, 1997), which is typical of calcareous soils. Also, the depression of root growth by HCO3– accounts for the calcifuge behavior of these plants (Peiter et al., 2001). Thus, the tolerance of lupins to Fe chlorosis seems to be related to their efficiency in solubilizing Fe, which, as stated above, is affected by the pH-buffering capacity of the soil (essentially determined by carbonates). Also, the amount of easily reducible Fe in the soil, which is essentially ascribed to poorly crystalline oxides, contributes to the Fe supply to roots. This is consistent with the hydroxylamine Fe predictions of chlorophyll meter readings at 3 wk (Table 6); in fact, it was the Fe extract related to poorly crystalline Fe fractions that showed the strongest relationship with the ACCE (Table 4).


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Hydroxylamine-extractable Fe provided the best estimation of chlorophyll content and dry matter production in white lupin grown in a representative group of calcareous soils from southern Spain. Iron in this extract was related to poorly crystalline Fe oxides and exhibited a stronger relationship with ACCE than other Fe extracts. This explains the merit of this method to predict the incidence of Fe chlorosis in this plant in the studied group of soils. This single extraction, easily reproducible, therefore provides an accurate estimate of available Fe content in the studied group of soils from southern Spain.


   ACKNOWLEDGMENTS
 
This work was funded by Spain's National R + D Plan (Project AGF2002-04134-CO2-01). We thank Dra. María del Carmen del Campillo for her invaluable advice during the conduct of the experiments and in reviewing the manuscript.

Received for publication October 10, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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A. de Santiago, I. Diaz, M. d. C. del Campillo, J. Torrent, and A. Delgado
Predicting the Incidence of Iron Deficiency Chlorosis from Hydroxylamine-Extractable Iron in Soil
Soil Sci. Soc. Am. J., August 20, 2008; 72(5): 1493 - 1499.
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