Journal of Experimental Botany, Vol. 52, No. 358, pp. 1093-1099,
May 1, 2001
© 2001 Oxford University Press
Original Papers |
Phytosiderophore release in Aegilops tauschii and Triticum species under zinc and iron deficiencies
1 Cukurova University, Department of Soil Science and Plant Nutrition, 01330 Adana, Turkey
2 Universität Hohenheim, Institut für Pflanzenernährung (330), 70593 Stuttgart, Germany
3 CIMMYT, POB 39, Emek 06511, Ankara, Turkey
4 Sabanci University, Faculty of Engineering and Natural Sciences, 81474 Tuzla, Istanbul, Turkey
Received 2 August 2000; Accepted 27 November 2000
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Using three diploid (Triticum monococcum, AA), three tetraploid (Triticum turgidum, BBAA), two hexaploid (Triticum aestivum and Triticum compactum, BBAADD) wheats and two Aegilops tauschii (DD) genotypes, experiments were carried out under controlled environmental conditions in nutrient solution (i) to study the relationships between the rates of phytosiderophore (PS) release from the roots and the tolerance of diploid, tetraploid, and hexaploid wheats and Ae. tauschii to zinc (Zn) and iron (Fe) deficiencies, and (ii) to assess the role of different genomes in PS release from roots under different regimes of Zn and Fe supply. Phytosiderophores released from roots were determined both by measurement of Cu mobilized from a Cu-loaded resin and identification by using HPLC analysis. Compared to tetraploid wheats, diploid and hexaploid wheats were less affected by Zn deficiency as judged from the severity of leaf symptoms. Aegilops tauschii showed very slight Zn deficiency symptoms possibly due to its slower growth rate. Under Fe-deficient conditions, all wheat genotypes used were similarly chlorotic; however, development of chlorosis was first observed in tetraploid wheats. Correlation between PS release rate determined by Cu-mobilization test and HPLC analysis was highly significant. According to HPLC analysis, all genotypes of Triticum and Ae. tauschii species released only one PS, 2'-deoxymugineic acid, both under Fe and Zn deficiency. Under Zn deficiency, rates of PS release in tetraploid wheats averaged 1 µmol (30 plants)-1 (3 h)-1, while in hexaploid wheats rate of PS release was around 14 µmol (30 plants)-1 (3 h)-1. Diploid wheats and Ae. tauschii accessions behaved similarly in their capacity to release PS and intermediate between tetraploid and hexaploid wheats regarding the PS release capacity. All Triticum and Aegilops species released more PS under Fe than Zn deficiency, particularly when the rate of PS release was expressed per unit dry weight of roots. On average, the rates of PS release under Fe deficiency were 3.0, 5.7, 8.4, and 16 µmol (30 plants)-1 (3 h)-1 for Ae. tauschii, diploid, tetraploid and hexaploid wheats, respectively. The results of the present study show that the PS release mechanism in wheat is expressed effectively when three genomes, A, B and D, come together, indicating complementary action of the corresponding genes from A, B and D genomes to activate biosynthesis and release of PS.
Key words: Aegilops tauschii, iron deficiency, phytosiderophores, Triticum monococcum, Triticum dicoccum, Triticum aestivum, zinc deficiency.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Zinc and Fe deficiencies are common micronutrient deficiencies in calcareous soils, and adversely affect crop production (Sillanpää, 1982
; Vose, 1982; White and Zasoski, 1999). Zinc deficiency is a particular micronutrient deficiency problem in cereal-growing areas causing large decreases in grain yield and quality, for example in Australia (Graham et al., 1992), Turkey (Cakmak et al., 1996a, 1999a) and India (Takkar et al., 1989).
There is substantial variation in tolerance to Zn or Fe deficiency within and among cereal species. Possibly, the release of phytosiderophores (PS) (non-protein amino acids) from roots in response to Fe or Zn deficiencies is an important factor affecting genotypic variation in the tolerance to Zn and Fe deficiencies. Phytosiderophores are highly effective in solubilization and mobilization of Zn and Fe in calcareous soils (Treeby et al., 1989) and are involved in the uptake of these nutrients by roots (Römheld and Marschner, 1990; von Wiren et al., 1995). The existence of large differences in tolerance to Fe deficiency between various cereal species correlated well with the release rate of PS from roots (Marschner et al., 1986; Kawai et al., 1988; Römheld and Marschner, 1990). Similarly, differences in tolerance to Zn deficiency between sorghum, wheat and corn correlate well with the amounts of PS released from roots (Hopkins et al., 1998). Wild grasses, adapted to severely Zn-deficient calcareous soils, released high amounts of PS when grown under Zn deficiency (Cakmak et al., 1996c). Bread wheat cultivars show greater tolerance to Zn deficiency than durum wheat cultivars, and this difference in tolerance correlated with differences in the release rate of phytosiderophores (Cakmak et al., 1994; Walter et al., 1994; Rengel et al., 1998). However, when genotypes of a given cereal species were compared, tolerance to Zn or Fe deficiencies and the rate of PS release were not always well correlated, as shown in oat for Fe deficiency (Hansen and Jolley, 1995) and wheat for Zn deficiency (Erenoglu et al., 1996).
Little information is available about the genetic control of PS release from roots. Since both the concentrations in roots and the amounts released from roots of PS are much lower in tetraploid (BBAA) than hexaploid wheats (BBAADD) under Fe and especially Zn deficiency (Cakmak et al., 1994, 1996b; Rengel and Romheld, 2000a), it can be assumed that the D genome possibly affects the biosynthesis and release of PS. Recently, it has been shown that diploid wheats (AA), like hexaploid wheats, possess very high tolerance to Zn deficiency when grown in Zn-deficient calcareous soils (Cakmak et al., 1999b). This may suggest a role of the A genome in the synthesis and release of PS. Aegilops tauschii (DD) is the donor of the D genome in hexaploid wheat (Kerby and Kuspira, 1987; Miller, 1987), and there is a high variation in tolerance to Zn deficiency between the accessions of Ae. tauschii (Cakmak et al., 1999c). Using only one genotype from each wheat species, it was recently shown (Ma et al., 1999) that diploid (AA), tetraploid (BBAA) and hexaploid wheats (BBAADD) and Ae. tauschii (DD) are able to release PS under Fe deficiency. In this study (Ma et al., 1999), the highest and lowest amounts of PS release were found in hexaploid and diploid wheats, respectively. In the present study, using three diploid (AA), three tetraploid (BBAA) and two hexaploid (BBAADD) wheats and two Ae. tauschii (DD) accessions experiments were carried out to study the role of different genomes on the release of PS under Fe and Zn deficiencies. Among the species studied, the diploid and hexaploid wheat genotypes are known to be tolerant to Zn deficiency, and tetraploid wheats and Ae. tauschii accessions show high and moderate sensitivity to Zn deficiency when grown on a severely Zn-deficient soil, respectively (Cakmak et al., 1999b, c).
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant growth
Two separate experiments were carried out to study the effects of genomes of the Ae. tauschii and Triticum species on PS release under Zn (experiment I) and Fe (experiment II) deficiencies. The genotypes of Ae. tauschii and Triticum species used in the present work are presented in Table 1
. Seeds from Germany were provided by Dr CI Kling (University of Hohenheim-Stuttgart). Seeds, surface-sterilized by 1% (v/v) sodium hypochlorite for 20 min, were germinated in quartz sand moistened with saturated CaSO4 solution. After 4 or 5 d the seedlings were transferred to 2.5 l plastic pots (30 seedlings per pot) containing the following continuously aerated nutrient solution: 0.88 mM K2SO4, 2.0 mM Ca(NO3)2, 0.25 mM KH2PO4, 1.0 mM MgSO4, 0.1 mM KCl, 1 µM H3BO4, 0.5 µM MnSO4, and 0.02 µM (NH4)6Mo7O24. In the experiment dealing with Zn deficiency no Zn, but 0.1 mM Fe-EDTA was added, and in the experiment with Fe deficiency, plants were supplied with 1 µM Fe-EDTA and 1 µM ZnSO4. Due to a limited number of seeds, experiments were carried out only under Zn- and Fe-deficient conditions with three replications for each genotype. Plants were grown for 21 d (Zn-deficient plants) and 13 d (Fe-deficient plants) in nutrient solution under controlled climatic conditions (light/dark regimes of 16/18 h, temperature 24/20 °C and photosynthetic photon flux of 350 µmol m-2 s-1 at plant height provided by Osram Sylvania cool white FR 96 T12 tubes, Ontario-Canada).
|
Collection of root exudates and measurement of PS
On days 10, 14, 18, and 21 for Zn-deficient plants and 9, 11 and 13 for Fe-deficient plants root exudates were collected for the measurement of PS release from roots. For the collection of root exudates, intact plants were removed from the nutrient solution 2 h after the onset of the light period, and then the roots were repeatedly washed in deoinized water and transferred to 500 ml aerated deionized water for 3 h. After the collection of root exudates, Micropur (Roth GmbH, Karlsruhe-Germany) was added into root exudates (10 mg l-1 of root exudate) to prevent microbial degradation of phytosiderophores. Thereafter, exudate solutions were filtered through course filter paper and concentrated to 20 ml at 50 °C under vacuum for Cu-mobilization test and HPLC analysis.
The amount of PS in the root exudates was determined indirectly by measurement of Cu mobilized from a Cu-loaded resin (Chelite-N, diameter 0.05–0.1 mm, Serva, Heidelberg, Germany) and calculated as mobilized Cu equivalents per plant or g-1 dry wt. Preparation of the Cu-loaded resin was described elsewhere (Cakmak et al., 1996b). Separation and identification of PS were achieved by HPLC on resin-based anion exchange columns using gradient eluation with aqueous NaOH (Neumann et al., 1999).
Shoot and root concentrations of Zn and Fe
At harvest, plants were separated into roots and shoots and washed several times with deionized water. After drying at 70 °C, samples were ground and ashed at 550 °C for 8 h. The ash was dissolved in 3.3% (v/v) HCl, and Zn and Fe concentrations were determined by atomic absorption spectrometry.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant growth and PS release under Zn deficiency
Average shoot dry weights of hexaploid and tetraploid wheats were very similar under Zn deficiency (Table 2
). However, the genotypes within each species showed greater variation regarding shoot dry weight. Also, average root dry weights of diploid, tetraploid and hexaploid wheats were similar, but differed between genotypes of each species, particularly in the case of T. dicoccum (Table 2). Among all genotypes of wheat species, FAL-02 showed the greatest shoot and root dry weights. Aegilops tauschii accessions had the lowest shoot and root dry weight. Visual Zn deficiency symptoms, such as reduction in plant height and appearance of whitish-brown necrotic patches on leaves, developed first in tetraploid wheats (BBAA). These symptoms appeared after 10 d of growth and became more severe with time. Of all T. dicoccum genotypes, FAL-02 was the least affected genotype as judged from the severity of visual Zn deficiency symptoms. In hexaploid and diploid wheats, Zn deficiency symptoms appeared 2 or 3 d later than that of tetraploid wheats and developed slightly. Aegilops tauschii is a wild wheat species and had a slower growth rate compared to the primitive and cultivated wheats. Therefore, in the Ae. tauschii accessions Zn deficiency symptoms developed slightly; however, at the end of the experiment Ae. tauschii accessions were also severely affected by Zn deficiency. Zinc concentrations of shoots and roots were very low, ranging between 7–9 mg kg-1 dry wt for shoots and 8–12 mg kg-1 dry wt for roots (Table 2).
|
There was a highly significant positive correlation (R2=0.89) between HPLC analysis and the results of the Cu-mobilization test (Fig. 1
), indicating this test as a simple and rapid method for PS analysis in root exudates. Therefore the amounts of PS released from roots were measured by this method. According to HPLC analysis, all genotypes of Aegilops tauschii and Triticum species used released only one PS, namely 2'-deoxymugineic acid, under both Zn and Fe deficiencies.
|
Under Zn-deficient conditions, the rate of PS release greatly varied depending on wheat genomes and plant age (Table 3
). During the 21 d of growth under Zn deficiency, the rate of PS release showed first a slight increase and then decreased and remained at a low level in tetraploid wheats and Ae. tauschii accessions. In the diploid and, particularly, hexaploid wheats the rate of PS release was high. While Bezostaja was an exception, PS release generally increased with the development of Zn deficiency symptoms (Table 3). When the rate of PS release was expressed per unit root dry weight, hexaploid and tetraploid wheats showed the highest and lowest rate of PS release, respectively. Based on the PS release per root dry weight, hexaploid wheats released about 14-fold more PS from roots than tetraploid wheats (Table 3).
|
Among the genotypes of each species there were differences in rate of PS release. For example, among the T. dicoccum genotypes, FAL-02 showed the highest rate of PS release, and among the hexaploid wheats primitive wheat T. compactum released higher amounts of PS than the modern hexaploid wheat Bezostaja. Of the Ae. tauschii accessions, 400682 was superior to 400630 in rate of PS release (Table 3
).
Plant growth and PS release under Fe deficiency
Under Fe deficiency, leaf chlorosis appeared on days 7 to 8 of growth in nutrient solution. Development of leaf chlorosis was observed first in the genotypes of tetraploid wheats, followed by the genotypes of other wheat species and Ae. tauschii. Average shoot dry weights of diploid, tetraploid and hexaploid wheats were similar under Fe deficiency, i.e. 24, 29 and 31 mg per plant, respectively (Table 4). However, within a given species genotypes tended to be different in their shoot dry weight, especially in the case of T. dicoccum. Among all species Aegilops tauschii showed the lowest shoot and root dry weight. Shoot Fe concentrations of plants under Fe deficiency were similar between Triticum and Ae. tauschii species, and ranged from 44 mg kg-1 dry wt (T. dicoccum and T. tauschii) to 49 mg kg-1 dry wt (T. monococcum and T. aestivum) (data not shown).
|
When compared with Zn deficiency (Table 3
), Fe deficiency caused greater increases in rate of PS release during 13 d of growth, especially per unit of root dry weight (Table 5). On day 13, the highest rate of PS release expressed per 30 plants was found in hexaploid wheats, followed by tetraploid and diploid wheats and Ae. tauschii. In contrast to the results obtained under Zn deficiency (Table 3), rates of PS release were, on average, higher in tetraploid wheats than those of diploid wheats (Table 5).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
When grown under non-stressed conditions, tetraploid wheats (BBAA) generally produce highest shoot dry weight, followed by hexaploid (BBAADD) and diploid wheats (AA) (Bamakramah et al., 1984
; Cakmak et al., 1999b). However, under Zn-deficient conditions, a decrease in shoot growth is much greater in tetraploid wheats than diploid and hexaploid wheats, indicating higher sensitivity of tetraploid wheats to Zn deficiency. Readers are referred to Cakmak et al. for detailed information about the effects of varied Zn supply on shoot dry matter production of diploid, tetraploid and hexaploid wheats in Zn-deficient calcareous soils (Cakmak et al., 1999b).
Compared to hexaploid wheats (BBAADD), tetraploid wheats (BBAA) released much less PS under Fe and, particularly, Zn deficiency (Tables 3, 5). This result is in agreement with the results obtained with different tetraploid and hexaploid wheats (Cakmak et al., 1994, 1996b; Rengel et al., 1998; Rengel and Römheld, 2000a). The low rate of PS release under Zn deficiency was considered as an important reason for high sensitivity of tetraploid wheats to Zn deficiency. As was also observed in the present study, tetraploid wheats appeared to be more sensitive to Fe deficiency than hexaploid wheats (Rengel and Römheld, 2000b). Release of PS at lower rates might be one factor contributing to the higher sensitivity of tetraploid wheats to Fe deficiency compared to hexaploid wheats. However, the role of PS in expression of high tolerance to Zn or Fe deficiency should be evaluated carefully. It has also been reported that bread wheat cultivars showing very high sensitivity to Zn deficiency, like durum wheats, released PS at rates as high as those of the Zn deficiency-tolerant bread wheat cultivars (Erenoglu et al., 1996; Cakmak et al., 1998).
Diploid wheats (AA) are very tolerant to Zn deficiency when grown in Zn-deficient calcareous soils (Cakmak et al., 1999b), and the transfer of the whole A genome from diploid wheat T. monococcum to tetraploid wheat (BBAA) T. turgidum markedly enhanced tolerance to Zn deficiency and improved growth under Zn deficiency (Cakmak et al., 1999d). Despite their high tolerance to Zn deficiency, diploid wheats (AA) did not release PS from roots at rates as high as those of hexaploid wheats (BBAADD) (Table 3). Even under Fe deficiency, diploid wheats generally released much less PS as compared with tetraploid and hexaploid wheats (Table 5). Therefore, it can be suggested that high tolerance of diploid wheats to Zn deficiency is not directly related to release of PS from roots, as proposed previously (Cakmak et al., 1999b, d). The reason for high tolerance of diploid wheats to Zn deficiency needs to be explained by mechanisms other than PS release, such as root uptake of Zn and its distribution and/or cellular compartmentation within plants.
Similar to diploid wheat genotypes, Ae. tauschii (DD) genotypes were not effective in the release of PS from roots under either Zn or Fe deficiency. These results suggest that the D and A genomes alone cannot solely contribute to the release of PS from the roots of wheats under Fe or Zn deficiency. When expressed per plant, the rate of PS release in wheat species under Fe deficiency decreased in the order:
T. aestivum (BBAADD)>T. dicoccum (BBAA)>
T. monococcum (AA)>Ae. tauschii (DD)
Recently, the same order has been shown (Ma et al., 1999) under Fe deficiency using only one genotype from each wheat species. However, in the case of Zn deficiency, the order of PS release was not similar to that found under Fe deficiency. PS release under Zn deficiency decreased in the following order:
T. aestivum (BBAADD)>T. monococcum (AA)>
Ae. tauschii (DD)>T. dicoccum (BBAA)
All wheat genomes carry genes affecting the biosynthesis and release of PS from roots. However, these genes are expressed predominantly and much more effectively when three genomes A, B and D are present together. This indicates the importance of complementary action of the corresponding genes from A, B and D genomes to activate the biosynthesis and release of PS in wheat. All these genomes were, to different extents, responsible for production of only one phytosiderophore, 2'-deoxymugineic acid (DMA). This result is in full agreement with the results published earlier (Ma et al., 1999). 2'-Deoxymugineic acid acts as a key precursor in biosynthesis of other phytosiderophores and is the major PS in root exudates of wheats (Mori et al., 1990; Ma and Nomoto, 1996).
When compared with tetraploid wheats (BBAA), diploid wheats (AA) released higher PS under Zn deficiency (Table 3). This result may suggest that the A genome has a greater importance than the B genome in the release of PS under Zn deficiency. Since tetraploid wheats with high sensitivity to Zn deficiency (Graham et al., 1992; Cakmak et al., 1996a; Rengel and Römheld, 2000b) consistently showed a low rate of PS release in a number of studies (Table 2; Cakmak et al., 1994, 1996b; Walter et al., 1994; Erenoglu et al., 1996; Rengel et al., 1998; Rengel and Römheld, 2000a) it might be suggested that the B genome of tetraploid wheats possess suppressor genes under Zn-deficient conditions; these suppressor genes possibly repress expression of the genes affecting biosynthesis and release of PS. This effect of Zn deficiency seems to be specific, because in the case of Fe deficiency, the rate of PS release from roots of tetraploid wheats is still fairly high and comparable with those found with hexaploid wheats. In future, studies should focus on a better understanding of the roles of the A, B and D genomes in the release of PS under Zn-deficient conditions by using tetraploid wheats with added A or D genomes (synthetic wheats) and accessions of Ae. speltoides and Ae. searsi which are considered the most probable donors of the B genome to tetraploid (BBAA) and hexaploid (BBAADD) wheats (Feldmann and Kislev, 1977; Kerby and Kuspira, 1987; Daud and Gustafson, 1996).
|
Acknowledgments |
|---|
This work was supported by the TUBITAK (Scientific and Technical Research Council of Turkey) and DFG (Deutsche Forschungsgemeinschaft).
|
Notes |
|---|
5 To whom correspondence should be addressed. Fax: +90 216 4839550. E-mail: cakmak{at}sabanciuniv.edu
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bamakhramah HS, Halloran GH, Wilson JH. 1984. Components of yield in diploid, tetraploid and hexaploid wheats (Triticum spp.). Annals of Botany 54, 51–60.
Cakmak I, Cakmak O, Eker S, Ozdemir A, Watanabe N, Braun HJ. 1999d. Expression of high zinc efficiency of Aegilops tauschii and Triticum monococcum in synthetic hexaploid wheats. Plant and Soil 215, 203–209.
Cakmak I, Gulut KY, Marschner H, Graham RD. 1994. Effect of zinc and iron deficiency on phytosiderophore release in wheat genotypes differing in zinc efficiency. Journal of Plant Nutrition 17, 1–17.
Cakmak I, Kalayci M, Ekiz H, Braun HJ, Yilmaz A. 1999a. Zinc deficiency as a practical problem in plant and human nutrition in Turkey: a NATO-Science for Stability Project. Field Crops Research 60, 175–188.
Cakmak I, Oztürk L, Karanlik S, Marschner H, Ekiz. H. 1996c. Zinc-efficient wild grasses enhance release of phytosiderophores under zinc deficiency. Journal of Plant Nutrition 19, 551–563.
Cakmak I, Sari N, Marschner H, Kalayci M, Yilmaz A, Braun HJ. 1996b. Phytosiderophore release in bread and durum wheat genotypes differing in zinc efficiency. Plant and Soil 180, 183–189.
Cakmak I, Tolay I, Ozdemir A, Ozkan H, Kling CI. 1999b. Differences in zinc efficiency among and within diploid, tetraploid and hexaploid wheats. Annals of Botany 84, 163–171.
Cakmak I, Tolay I, Ozkan H, Ozdemir A, Braun HJ. 1999c. Variation in zinc efficiency among and within Aegilops species. Journal of Plant Nutrition and Soil Science 162, 257–262.
Cakmak I, Torun B, Erenoglu B, Oztürk L, Marschner H, Kalayci M, Ekiz H, Yilmaz A. 1998. Morphological and physiological differences in cereals in response to zinc deficiency. Euphytica 100, 349–357.
Cakmak I, Yilmaz A, Ekiz H, Torun B, Erenoglu B, Braun HJ. 1996a. Zinc deficiency as a critical nutritional problem in wheat production in Central Anatolia. Plant and Soil 180, 165–172.
Daud HM, Gustafson JP. 1996. Molecular evidence for Triticum speltoides as a B-genome progenitor of wheat (Triticum aestivum). Genome 39, 543–548.
Erenoglu B, Cakmak I, Marschner H, Römheld V, Eker S, Daghan H, Kalayci M, Ekiz H. 1996. Phytosiderophore release does not correlate well with zinc efficiency in different bread wheat genotypes. Journal of Plant Nutrition 19, 1569–1580.
Feldman M, Kislev M. 1977. Aegilops searsii, a new species of the section Sitopsis (Platystachys). Israel Journal of Botany 26, 190–201.
Graham RD, Ascher JS, Hynes SC. 1992. Selecting zinc-efficient cereal genotypes for soils of low zinc status. Plant and Soil 146, 241–250.
Hansen NC, Jolley VD. 1995. Phytosiderophore release as a criterion for genotypic evaluation of iron efficiency in oat. Journal of Plant Nutrition 18, 455–465.
Hopkins BG, Whitney DA, Lamond RE, Jolley VD. 1998. Phytosiderophore release by sorghum, wheat, and corn under zinc deficiency. Journal of Plant Nutrition 21, 2623–2637.
Kawai S, Takagi S, Sato Y. 1988. Mugineic acid-family phytosiderophores in root secretions of barley, corn and sorghum varieties. Journal of Plant Nutrition 11, 633–642.
Kerby K, Kuspira J. 1987. The phylogeny of the polyploid wheats Triticum aestivum (bread wheat) and Triticum turgidum (macaroni wheat). Genome 29, 722–737.
Ma JF, Nomoto K. 1996. Effective regulation of iron acquisition in graminaceous plants. The role of mugineic acids as phytosiderophores. Physiologia Plantarum 97, 609–617.
Ma JF, Taketa SY, Chang K, Takeda, Matsumoto H. 1999. Biosynthesis of phytosiderophores in several Triticeae species with different genomes. Journal of Experimental Botany 50, 723–726.
Marschner H, Römheld V, Kissel M. 1986. Different strategies in higher plants in mobilization and uptake of iron. Journal of Plant Nutrition 9, 695–713.[Web of Science]
Miller TE. 1987. Systematics and evolution. In: Lupton FGH, ed. Wheat breeding. Chapman and Hall, New York, 1–30.
Mori S, Nishizawa N, Fujigaki J. 1990. Identification of rye chromosome 5R as a carrier of the genes for mugineic acid synthetase and 3-hydroxymugineic acid synthetase using wheat-rye addition lines. Japanase Journal of Genetics 65, 343–352.
Neumann G, Haake C, Römheld V. 1999. Improved HPLC method for determination of phytosiderophores in root washings and tissue extracts. Journal of Plant Nutrition 22, 1389–1402.[Web of Science]
Rengel Z, Römheld V. 2000a. Root exudation and Fe uptake and transport in wheat genotypes differing in tolerance to Zn deficiency. Plant and Soil 222, 25–34.
Rengel Z, Römheld V. 2000b. Differential tolerance to Fe and Zn deficiencies in wheat germplasm. Euphytica 113, 219–225.
Rengel Z, Romheld V, Marschner H. 1998. Uptake of zinc and iron by wheat genotypes differing in tolerance to zinc deficiency. Journal of Plant Physiology 152, 433–438.
Römheld V, Marschner H. 1990. Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores. Plant and Soil 123, 147–153.
Sillanpää M. 1982. Micronutrients and the nutrient status of soils. A global study. FAO Soils Bulletin (No. 48), FAO, Rome.
Takkar PN, Chibba IM, Mehta SK. 1989. Twenty years of coordinated research of micronutrients in soil and plants (1967–1987). Indian Institute of Soil Science, Bhopal, IISS, Bull. I.
Treeby M, Marschner H, Römheld V. 1989. Mobilization of iron and other micronutrient cations from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant and Soil 114, 217–226.[Web of Science]
von Wiren N, Marschner H, Römheld V. 1996. Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiology 111, 1119–1125.[Abstract]
Vose PB. 1982. Iron nutrition in plants: a world overview. Journal of Plant Nutrition 5, 233–249.[Web of Science]
Walter A, Römheld V, Marschner H, Mori S. 1994. Is the release of phytosiderophores in zinc-deficient wheat plants a response to impaired iron utilization? Physiologia Plantarum 92, 493–500.
White JG, Zasoski RH. 1999. Mapping soil micronutrients. Field Crops Reearch 60, 11–26.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. R. Meda, E. B. Scheuermann, U. E. Prechsl, B. Erenoglu, G. Schaaf, H. Hayen, G. Weber, and N. von Wiren Iron Acquisition by Phytosiderophores Contributes to Cadmium Tolerance Plant Physiology, April 1, 2007; 143(4): 1761 - 1773. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. A. Roberts, A. J. Pierson, Z. Panaviene, and E. L. Walker Yellow Stripe1. Expanded Roles for the Maize Iron-Phytosiderophore Transporter Plant Physiology, May 1, 2004; 135(1): 112 - 120. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Schaaf, U. Ludewig, B. E. Erenoglu, S. Mori, T. Kitahara, and N. von Wiren ZmYS1 Functions as a Proton-coupled Symporter for Phytosiderophore- and Nicotianamine-chelated Metals J. Biol. Chem., March 5, 2004; 279(10): 9091 - 9096. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||