Cycling silicon – the role of accumulation in plants
2003; Wiley; Volume: 158; Issue: 3 Linguagem: Inglês
10.1046/j.1469-8137.2003.00778.x
ISSN1469-8137
Autores Tópico(s)Geochemistry and Elemental Analysis
ResumoSilicon, the element in so many plant scientists' minds as we come into an age of research 'in silico', still presents an enigma when it comes to its nutritional role in higher land plants. We should all be well aware of it – the second most abundant element in the Earth's crust, which occurs in the soil solution at 0.1–0.6 mol m−3 as Si(OH)4 (two orders of magnitude higher than the macronutrient phosphorus occurs as H2PO4−/HPO42––Epstein, 1999; Datnoff et al., 2001). Yet silicon is not an essential element for any of the embryophytes tested, and the dry matter of these contains very variable amounts of the element – 1.3–47.3 mg per g of plant dry matter (Epstein, 1999; Ma et al., 2001). Essential, in strict plant nutritional terms, means that the plant cannot complete its life cycle, under otherwise optimal conditions, in as near to the absence of the element as techniques will allow. Clearly we need to know more about the role of silicon in plants, and in this issue (pp. 431–436) Tamai & Ma address the most basic of questions – how does the silicon get into the plant in the first place? (see also Lux et al. pp. 437–441 in this issue, who have examined silicon in sorghum). The study species used by Tamai & Ma, rice, is an especially intriguing case because, as is well known, rice is a major silicon accumulator. While silicon is not essential for the growth of higher plants, we do know that its availability influences many aspects of the biology of plants that naturally have moderate to high levels of the element (Epstein, 1999; Datnoff et al., 2001). Examples are restriction of grazing and parasitism, increased light interception, and alleviation of the effects of deficiency or excess of nutrient and other solutes (Epstein, 1999; Datnoff et al., 2001; Britez et al., 2002). Thus, although silicon is not essential for higher plants it very significantly improves fitness in nature and increases agricultural productivity. Photosynthetic organisms other than higher plants can also have an important involvement with silicon. Of these the most globally significant are the diatoms (Bacillariophyceae: Heterokontophyta), with an absolute requirement. Cell walls, or frustules, of diatoms are silicified – among the roles of these silicified walls is that of mechanical protection from grazers (Hamm et al., 2003). Plants (in the broad sense) are not only involved with silicon in terms of growth, but are also major components of the global silicon cycle. Taking the land surface as a starting point, vascular plants play a major role in weathering silicate rocks (Berner & Berner, 1996; Lucas, 2001; Raven & Edwards, 2001). 'Biological pumping' of CO2 from the bulk atmosphere to the soil atmosphere involves photosynthesis by shoots, translocation of organic carbon to the roots, and respiration by plants and soil biota of living and dead plant material (Lucas, 2001). The restricted diffusion pathway to the bulk atmosphere gives a steady state CO2 concentration in the soil atmosphere which is one or two orders of magnitude higher than that in the bulk atmosphere. The high concentration of CO2 in the soil solution increases the rate at which CO2 reacts with silicate rocks to yield soluble silicic acid and the soluble bicarbonate salts of the metals from the silicates (Berner & Berner, 1996; Lucas, 2001). Most soil solution water ultimately reaches the ocean, providing, with a minor component from the reaction of seawater with basalt, the silicic acid input to the oceans. Silicic acid is removed from the ocean by long-term incorporation into sediments of a small fraction (a few per cent) of the biogenic silica which is precipitated in intracellular compartments after active influx of silicic acid in, predominantly, planktonic diatoms (Berner & Berner, 1996; Falkowski & Raven, 1997; De Master, 2002). Most of the silica produced by diatoms is recycled to silicic acid in the ocean water. The cycle of silicon is completed by reactions at high temperature and pressure in the Earth's crust. Silica, with sedimented carbonates produced biologically from bicarbonate, is reconverted to metal silicates that ultimately return to the Earth's surface with production of CO2– which then returns to the atmosphere via volcanoes (Berner & Berner, 1996). The global rate of silicate weathering (plus the basalt seawater reaction) and of deposition of biogenic silica in marine sediments is in excess of 200 Tg Si (7 Tmol Si) per year. While the predominant role of photosynthetic organisms in the silicon cycle is in converting silicates to silicic acid on land and converting silicic acid to silica in the ocean, terrestrial higher plants are also involved in the conversion of silicic acid to silica (Raven, 1983; Datnoff et al., 2001). Silicic acid enters the plants, as does water, and is carried in the transpiration stream toward transpiration termini (Canny, 1994). As water evaporates, silicic acid becomes supersaturated with respect to solid hydrated silica, which is precipitated as phytoliths. Ultimately these phytoliths are resolubilized and join the flux of silicic acid to the ocean. It is these silica deposits which give the increased resistance to grazers and parasites and changed leaf posture in many of the plants already mentioned (Datnoff et al., 2001). The quantity of silica that is deposited per unit dry matter gained depends on the quantity of silicic acid per unit water transpired and the quantity of water transpired per unit dry matter gain. Ma et al. (2001) point out that a 'typical' soil solution concentration of silicic acid of 0.35 mol m−3, and 500 g water transpired per g dry matter increase in a C3 plant, would yield 5 mg Si per g dry matter if the silicic acid and water were taken up in the same proportion as in the soil solution. Ma et al. (2001) measured the Si content of the dry matter of a range of terrestrial embryophytes, and compared the values with the 5 mg Si per dry matter that they had calculated for proportional uptake of silicic acid and water from the soil solution. Of the plants that they tested, Ma et al. (2001) found that bryophytes (two species), lycopsids (two species), sphenopsids (two species), pteropsids (26 species), eight species from the Cucurbitales, five species from the Urticales, one species from the Eriocaulales, seven species from the Cyperales and 211 species from the Graminales had Si contents of at least 10 mg Si per g dry matter. These plants are silicon accumulators or, in the case of the Cucurbitales and Urticales, in an intermediate category between nonaccumulaters and accumulaters as judged from the relatively low Si : Ca ratio in the plants (Ma et al., 2001). The plants tested by Ma et al. (2001), which were nonaccumulators of silicon, were 25 species of pteropsids, 12 species of gymnosperms, and two species from the Cyperales. The 'nonaccumulators' actually exclude silicic acid from the plant, because they contain less silicon than would be expected if there was nonselective passive entry of silicic acid with water. By contrast, the accumulators (and intermediate plants) take up silicic acid faster than would be expected from a nonselective entry of silicic acid with water during plant growth. The plants which exclude silicic acid all have endodermes in their roots (Raven & Edwards, 2001), and so could readily exclude silicic acid relative to water. This could occur regardless of whether these compounds enter by uncatalysed movement across the lipid component of the plasmalemma or, probably, when they enter by aquaporins (Raven, 2001; Tyerman et al., 2002). The plants which accumulate silicic acid must use active transport across (a) membrane(s). These plants do not always have endodermes in their roots (e.g. the genus Lycopodium among Lycopsida) or other absorptive organs (e.g. below-ground parts of bryophytes) (Raven, 2001; Raven & Edwards, 2001). This absence of an apoplasmic barrier would limit the extent to which leakage back to the medium of solutes actively transported into the transpiration stream could be prevented (Raven & Edwards, 2001; Raven, 2001). Notwithstanding this problem, active transport must occur in these cases. For higher plants, the active transport occurs inwards at the plasmalemma of root epidermal or cortical cells (or mycorrhizas?) and/or outwards at the plasmalemma abutting on xylem elements. While there is a good understanding at the molecular genetic level of silicic acid active influx in diatoms (Hildebrand et al., 1997; Hildebrand et al., 1998), much less is known about silicic acid active transport in higher plants. In this issue, Tamai & Ma report on results that significantly advance our understanding of the mechanism of active influx of silicic acid into roots of rice. Their work on net uptake by whole plants confirmed that rice takes up silicic acid (on a root dry matter basis) an order of magnitude faster than any of the other six cereal species tested. The lack of effect of pretreatment with silicic acid led the authors to conclude that the silicic acid transport system was constitutive rather than inducible. The transporter taking up silicic acid has a relatively low affinity (half-saturation of 0.32 mmol m−3). Studies with inhibitors suggest that aquaporins are probably not involved in silicic acid transport, and that anion antiporters are almost certainly not involved. Inhibitor studies also suggest that the catalytic site(s) of the transporter involves cysteine but not lysine residues. This work, together with that of Ma et al., 2003, on a rice mutant which is defective in silicic acid uptake, provides a good basis for further work. Clearly we need more knowledge of how active transport of silicic acid occurs in higher plants. Especially important is better understanding of the high accumulation of silicon seen in rice, the single most important human food crop. In many rice-growing areas yields are significantly enhanced by fertilization with silicon fertilizers, in some cases as a result of prolonged silicon removal in the harvested crop (Datnoff et al., 2001). Finally, it is salutary to note that grasses and diatoms, with, respectively, a beneficial and an essential role for silicic acid, are very important in global net primary productivity. Grasses fix c. 15 Pg C per year out of c. 60 Pg C per year of net primary production on land, and diatoms fix > 15 Pg C per year out of c. 50 Pg C per year of net primary production in the ocean (Ajtay et al., 1979; Falkowski & Raven, 1997; Field et al., 1998).
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