Soil Science Society of America Journal 66:1265-1271 (2002)
© 2002 Soil Science Society of America
DIVISION S-5—PEDOLOGY
Origin of Silica Particles Found in the Cortex of Matteuccia Roots
FengFu Fu*,a,
Tasuku Akagib and
Sadayo Yabukia
a Division of Surface Characterization, The Institute of Physical and Chemical Research (RIKEN), Wako, Saitama 351-0198, Japan
b Faculty of Agriculture, Tokyo Univ. of Agriculture and Technology, Saiwai-cho 3-5-8, Fuchu, Tokyo 183-8509, Japan
* Corresponding author (fengfu{at}postman.riken.go.jp)
 |
ABSTRACT
|
|---|
A root sample from a species of fern (Matteuccia) was observed in detail under scanning electron microscopy (SEM), and some micron-sized particles were observed in the cortex. Energy-dispersive x-ray spectroscopy (EDX) analysis of the particles indicated that they were almost pure silica. The concentrations of rare earth elements (REEs) in the silica particles from the roots, and silicate mineral particles from the soil, were analyzed by inductively coupled plasma–mass spectrometry (ICP-MS). The REE composition of the silica particles from the roots was similar to that of the silicate mineral particles in the soil. The absence of a "Ce anomaly" in the REE patterns implies that the silica particles found in the cortex of Matteuccia roots were produced not by chemical deposition, but most likely by incorporation of silicate minerals into the root cortex and subsequent leaching of nutrient elements from the particles. This process is both a novel mechanism for plants to obtain nutrients and a means whereby plants accelerate the weathering of soil minerals.
Abbreviations: EDX, energy-dispersive x-ray spectroscopy • ICP-MS, inductively coupled plasma-mass spectometry • REE, rare earth elements • SEM, scanning electron microsopy
|
INTRODUCTION
|
|---|
SILICON OCCURS IN ALL plants, but it is unclear whether it is an essential nutrient for plant growth (Epstein, 1999). Scientists have been interested in the behavior and the role of Si in plants for many years (Takahashi et al., 1981; Jarvis, 1987a,b; Epstein, 1994; Cocker et al., 1998a,b). It is generally thought that Si is absorbed by plants in a dissolved form (silicic ion) from solution. Plant opals, observed in leaves from Si-accumulating plants (for example, Gahnia sieberana, Entolasia stricta, and Pteridium esculentum), are generally considered to be produced from dissolved Si in a plant body (Smithson, 1956; Hart, 1988; Sato et al., 1990; Herbauts et al., 1994; Wang et al., 1998). An opaline form has been found in the roots of some genera, and nodular deposits of silica have been observed in the inner tangential wall of the endodermis of some plants' roots (Sangster, 1978). The origin of the opaline and nodular silica deposits in plant roots is still open to question.
Fu et al. (1998)(2000, 2001) have proposed the possibility that some plants may absorb silicate particles directly and selectively from the soil based on the similarity between the REE composition of plant roots and that of silicate particles in the soil. However, no direct observational evidence has been presented to support this hypothesis. In this study, we attempted to identify and determine the REE composition of silica particles in fern root sections to discuss their genesis and relationship with silicates in the soil.
|
MATERIALS AND METHODS
|
|---|
Scanning Electron Microscopy-Energy Dispersive X-ray Observations of Matteuccia Roots
Relatively large sections of Matteuccia roots were sampled in 1998 from a site on the campus of the Tokyo University of Agriculture & Technology (Fuchu, Tokyo, Japan). The samples were thoroughly washed with Milli-Q water to remove soil attached to the external surface of the root and then dried at 105°C. One section of the dried root was cut along the axis and one half of the section was analyzed by SEM-EDX. To do so, the sample was mounted on an SEM stud and then coated with a thin layer of carbon. The sample was analyzed using a JEOL JSM6330F SEM (Tokyo, Japan) equipped with a JED-2200 EDX unit using an accelerating voltage of 10 kV, a working distance of 15 mm, and a 12-µA probe current. Under x2000 magnification, the cortex surface was scanned for micron-sized particles. A semi-quantitative elemental analysis was then performed on these particles using EDX.
Isolation of Silicate Particles from Roots and Determination of Rare Earth Elements
About 3 g of dried Matteuccia roots, whose epidermis was removed, were placed in a Teflon beaker (Dupont, Boston, MA) with 5 mL of 10 M HNO3 and 5 mL of 10 M HClO4. The Teflon beaker was gently heated until the roots were completely digested. The solution was evaporated to dryness by slowly heating the beaker, and the residue treated with 10 mL of 0.2 M HNO3. The solution was filtered through a 0.22-µm Millipore filter (Millipore Corp., Bedford, MA), and the residue dried at 100°C along with the filter. Part of the residue was used for analysis by SEM-EDX.
Another part of the residue (
0.005 g) was digested in 3 mL 1:1:1 mixture of HF/HNO3/HClO4, and then analyzed for REEs by ICP-MS as described by Fu et al. (1997).
Determination of Rare Earth Elements in Silicate Particles of Soil
Soil surrounding the Matteuccia roots was sampled from 15-cm depth on the same day of plant sampling. The soil was a typical Kanto loam (melanaquands), and had a pH (KCl) of 5. About 0.3 g of dried soil was placed in a Teflon beaker with 5 mL of 10 M HNO3 and 5 mL of 6 M HClO4, and slowly heated on a hot plate. After the acid solution became clear, it was evaporated to dryness by heating it slowly, and then the residue was treated with 10 mL of 0.2 M HNO3. The solution was filtered through a 0.22-µm Millipore filter, and the residue on the filter was dried at 100°C. The recovery of the residue from 0.3 g of dried soil was 0.10 g and REEs in the residue were determined by the same ICP-MS method used for the residue recovered from the Matteuccia roots.
|
RESULTS AND DISCUSSION
|
|---|
Compositions of Silicate Particles in Matteuccia Roots and Soil
The SEM images showed micron-size (0.5–1.5 µm) particles imbedded in the cortex of Matteuccia roots (Fig. 1)
. The EDX analysis of the particles (Fig. 2)
gave three dominant peaks, C, O, and Si, and three very small peaks, Ca, Mg, and K. The C peak is because of the carbon coating and the organic constituents of the root. Although it is not clear whether the small amounts of Ca, Mg, and K came from the particles or the roots, the analysis clearly showed that the particles were dominated by silica (SiO2). The SEM-EDX analysis of the residue from digested Matteuccia roots also showed that the residual particles were nearly pure silica (Fig. 3)
.
View larger version (127K):
[in this window]
[in a new window]
|
Fig. 1. Scanning electron microscopy (SEM) images of the vertical section of a relatively large Matteuccia root. Magnification is (A) x60 and the circled part of A is (B) x5000 magnification. The arrow shows an example of the micron-sized particles.
|
|
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 2. Energy-dispersive x-ray (EDX) analysis of the micron-sized particles shown by the arrow in Fig. 1B. All particles showed similar EDX results, as indicated by this example.
|
|
The SEM-EDX analysis of particles attached to the external surface of Matteuccia roots is shown in Fig. 4
. Peaks of C, O, Mg, Al, Si, K, and Ca were found for these particles, indicating that these particles were silicate minerals (MlSimOn) rather than silica. Analysis of 10 different particles embedded in the external surfaces of the root indicated that they all contained similar levels of Si, Al, Mg, K, and O.
View larger version (69K):
[in this window]
[in a new window]
|
Fig. 4. The scanning electron microscopy (SEM) image (x2500) of the particles attached to the external surface of the Matteuccia roots and energy-dispersive x-ray (EDX) analysis of the particles.
|
|
The silicate particles found on the external surfaces of the Matteuccia roots are assumed to have come from the surrounding soil which has 30% clay, and the clay is dominated by allophane but also contains quartz, feldspar, and other silicate minerals (Komamura and Takenaka, 1983). The residue obtained after acid digestion of the soil was dominated by silica but also contained small amounts of Al (Fig. 5)
. Plant opals are commonly observed in the soil; however, the amount of plant opal is generally a few miligram per gram of soil and is much smaller than the amount of silicate residue (0.3 g g-1 soil) recovered after the acid digest (Herbauts, 1994). Therefore, the existence of plant opals in the soil would not significantly affect the REE composition of the residue collected from the soil, which will be discussed later.
View larger version (77K):
[in this window]
[in a new window]
|
Fig. 5. Scanning electron microscopy (SEM) image (x1000) of the residual matter from 0.3 g of soils after treatment with 5 mL of HNO3 and 5 mL of HClO4, and energy-dispersive x-ray (EDX) analysis of the residue.
|
|
Source of Silica Particles in Matteuccia Roots
There are two possible interpretations for the source of silica particles found in Matteuccia roots.
1. Silicic ions may be taken up by the roots from the soil solution and then deposited in the endodermis as discrete silica nodules, or as plant opal (Sangster and Parry 1976; Sangster, 1978).
2. Silicate mineral particles from the soil may have been trapped in the wrinkles on the external surface of the root and then incorporated into the root cortex with root growth. Subsequently, the soluble elements (K+, Ca+, Mg+, etc.) were leached from the silicate mineral particles into the cortex and carried to the shoot as nutrients, leaving residual silica particles in the cortex.
To judge whether Interpretation 1 or 2 is true, we have compared the concentrations of REEs in the silica particles collected from the Matteuccia roots with that of the silicate particles collected from the soil using chondrite normalized REE patterns (Fig. 6)
. The REE pattern was drawn by plotting the relative abundance of each REE in the sample relative to that of a chondrite on a logarithmic scale against the atomic number. The REE abundances of chondrite used here were from Masuda et al. (1973) and Masuda (1975). The REE pattern of the silica particles collected from the Matteuccia roots and that of the silicate particles in the soil are almost identical, implying that the repartitioning of REE did not take place during the process responsible for the silica particles in the root cortex.
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 6. The REE pattern of silica particles from Matteuccia roots (A) and that of silicate particles extracted from the soil (B). The REE pattern is made by plotting the abundance of each REE in samples relative to that in a chondrite on a logarithmic scale against the atomic number of the REE. The normalizing values were from Masuda et al. (1973) and Masuda (1975).
|
|
Rare earth elements patterns are usually altered during the process of dissolution and reprecipitation. For instance, during dissolution, Ce is generally segregated from the other REEs as a solid oxide and, therefore, Ce is depleted from reprecipitated particles (negative Ce anomaly) (Akagi and Masuda, 1998). In addition, a tetrad effect is usually involved in the partitioning between dissolved species (Masuda et al., 1987). The tetrad effect creates a quite distinctive feature in the REE pattern: four contiguous curves in which each curve consists of four successive elements (La-Ce-Pr-Nd, (Pm)-Sm-Eu-Gd, Gd-Tb-Dy-Ho, Er-Tm-Yb-Lu). An example of the tetrad effect is shown in Fig. 7 , which was first observed in the partition coefficients of REEs in solvent extraction (Peppard et al., 1969). Our survey of REE composition in various species of plants has revealed that most plants show the Ce anomaly and the tetrad effect-like variation in the heavier REE region (Fu et al., 1998; Fu et al., 2000; Fu et al., 2001). The absence of the Ce anomaly and the tetrad effect in the REE pattern for the silica particles in the Matteuccia roots implies that these particles have not gone through the process of dissolution and reprecipitation. Therefore, the REE patterns are not consistent with Interpretation 1, but support Interpretation 2. The identical REE patterns of the silica particles collected from the Matteuccia roots and the silicate particles of the soil (Fig. 6) also imply that these particles have the same origin. Small Ca, K, and Mg EDX peaks observed for the silica particles in the cortex (Fig. 2) are also evidence supporting interpretation (2). This assumes that these three elements are not leached completely and that small amounts of these elements remained in the silicate mineral particles (silica particles) found in the root cortex.
View larger version (17K):
[in this window]
[in a new window]
|
Fig. 7. The tetrad effect observed in the partition of a solvent extraction system (Peppard et al., 1969). Relative element abundance stands for concentration ratio of aqueous to organic phase (reciprocal of partition coefficient). Solvent extraction system: 0.6 F DEH [CIMP] (benzene) vs. 11.4 F LiBr + 0.5 F HBr. Heavier REEs in most plants including Matteuccia showed tetrad effect-like variation unlike particles studied in this study.
|
|
This study not only presents a novel mechanism for the uptake of nutrients by plants, but also implies that plants may accelerate the process of soil mineral weathering. The soil mineralogy is greatly influenced by plant activity, and fresh silicate and clay minerals could be weathered to silica by the plants. This interpretation is compatible with recent reports that the weathering rate is accelerated by the presence of plants (Bormann et al., 1998).
|
CONCLUSION
|
|---|
Some micron-sized particles found in the cortex of Matteuccia roots were almost pure silica and were different from the silicate mineral particles attached to the external surface of Matteuccia roots. Rare earth element abundance in the silica particles indicates that no diagenetic alteration occurred during their formation, implying that the fern may physically incorporate silicate-mineral particles into the root cortex, dissolve inorganic nutrients from the silicate minerals and leave silica particles. When the plant dies, the newly formed silica particles are returned to the soil. This process represents a previously unrecognized pathway for the alteration of silicate minerals in soils.
Received for publication January 11, 2001.
|
REFERENCES
|
|---|
- Akagi, T., and A. Masuda. 1998. A simple thermodynamic interpretation of Ce anomaly. Geochem. J. 32:301–314.
- Bormann, B.T., D. Wang, F.H. Bormann, G. Benoit, R. April, and M.C. Snyder. 1998. Rapid, plant-induced weathering in an aggrading experimental ecosystem. Biogeochemistry 43:129–155.
- Cocker, K.M., D.E. Evans, and M.J. Hodson. 1998a. The amelioration of aluminium toxicity by silicon in wheat (Triticum aestivum L.): malate exudation as evidence for an in planta mechanism. Planta 204:318–323.
- Cocker, K.M., D.E. Evans, and M.J. Hodson. 1998b. The amelioration of aluminium toxicity by silicon in higher plants: solution chemistry or an in planta mechanism? Physiologia Plantarum 104:608–614.
- Epstein, E. 1994. The anomaly of silicon in plant biology. Proc. Natl. Acad. Sci. USA 91:11–17.[Abstract/Free Full Text]
- Epstein, E. 1999. Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:641–664.[ISI]
- Fu, F.-F., T. Akagi, and K. Shinotsuka. 1998. Distribution pattern of rare earth elements in fern: Implication for intake of fresh silicate particles by plants. Biol. Trace Elem. Res. 64:13–26.[ISI][Medline]
- Fu, F.-F., T. Akagi, S. Yabuki, and M. Iwaki. 2001. The variation of REE (rare earth elements) patterns in soil-grown plants: A new proxy for the source of rare earth elements and silicon in plants. Plant Soil 235:53–64.
- Fu, F.-F., T. Akagi, S. Yabuki, M. Iwaki, and N. Ogura. 2000. Distribution of rare earth elements in seaweed: Implication for two different sources of rare earth elements and silicon in seaweed. J. Phycol. 36:62–70.[ISI]
- Fu, F.-F., K. Shinotsuka, M. Ebihara, and T. Akagi. 1997. Distribution ratio of dissolved and particulate REE in surface coastal seawater. Geochem. J. 31:303–314.
- Hart, D.M. 1988. The plant opal content in the vegetation and sediment of a swamp at Oxford Falls, New South Wales, Australia. Aust. J. Bot. 36:159–170.
- Herbauts, J., F.A. Dehalu, and W. Gruber. 1994. Quantitative determination of plant opal content in soil, using a combined method of heavy liquid separation and alkali dissolution. Eur. J. Soil Sci. 45:379–385.
- Jarvis, S.C. 1987a. The uptake and transport of silicon by perennial ryegrass and wheat. Plant Soil 97:429–437.
- Jarvis, S.C. 1987b. The absorbtion and transport of manganese by perennial ryegrass and white clover as affected by silicon. Plant Soil 99:231–240.
- Komamura, M., and H. Takenaka. 1983. Engineering properties of Kanto volcanic ash soil—The phenomenon of softening or hardening and shrinkage of Kanto volcanic ash soil. p. 25–30. In Committee of Volcanic Ash and Soil (ed.) Volcanic ash and soil. (In Japanese.) Kokusai Printing Industry, Osaka, Japan.
- Masuda, A. 1975. Abundances of monoisotopic REE, consistent with Leedey chondrite values. Geochem. J. 9:183–184.
- Masuda, A., O. Kawakami, Y. Dohmoto, and T. Takenaka. 1987. Lanthanide tetrad effects in nature: Two mutually opposite types, W and M. Geochem. J. 21:119–124.
- Masuda, A., N. Nakamura, and T. Tanaka. 1973. Fine structures of mutually normalized rare earth patterns of chondrites. Geochim. Cosmochim. Acta 37:239–248.
- Peppard, D.F., G.W. Mason, and S. Lewey. 1969. A tetrad effect in the liquid-liquid extraction ordering of lanthanides (III). J. Inorg. Nucl. Chem. 31:2271–2272.
- Sangster, A.G. 1978. Silicon in the roots of higher plants. Am. J. Bot. 65:929–935.
- Sangster, A.G., and D.W. Parry. 1976. The ultrastructure and electron-probe microassay of silicon deposits in the endodermis of the seminal roots of Sorghum bicolor (L.) Moench. Ann. Bot. 40:447–459.[Abstract/Free Full Text]
- Sato, Y., H. Fujiwara, and T. Udatsu. 1990. Morphological differences in silica body derived from Motor cell of indica and japonica in rice. Jpn. J. Breed. 40:495–504.
- Smithson, F. 1956. Plant opal in soil. Nature 176:107.
- Takahashi, E., H. Tanaka, and Y. Miyake. 1981. Distribution of silicon accumulating plants in the plant kingdom. (In Japanese.) Jpn. J. Soil Sci. Plant Nutr. 52:511–515.
- Wang, C., T. Udatsu, L. Tang, J. Zhou, Y. Zheng, A. Sasaki, K. Yanagisawa, and H. Fujiwara. 1998. Cultivar group of rice cultivated in Caoxieshan Site (B. P. 6000present) determined by the morphology of plant opals and its historical change. Breed. Sci. 48:387–394.
TOP
ABSTRACT
INTRODUCTION
