Forum
Commentary
Blackwell Publishing Ltd.
Cycling silicon – the role of
accumulation in plants
Silicon, 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.
What do we know about silicon in plants?
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 moder-
ate to high levels of the element (Epstein, 1999; Datnoff
et al., 2001). Examples are restriction of grazing and para-
sitism, 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 (Bacillariophyc-
eae: 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).
© New Phytologist (2003) 158: 419 – 430 www.newphytologist.com
The global silicon cycle
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 atmo-
sphere 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 concentra-
tion 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 intra-
cellular 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 bicarbon-
ate, 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.
Converting silicic acid to silica in higher plants
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
419
420 Forum Commentary
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 resist-
ance 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.
Movement through the plant
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 Erio-
caulales, 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 pterop-
sids, 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 read-
ily exclude silicic acid relative to water. This could occur
regardless of whether these compounds enter by uncata-
lysed movement across the lipid component of the plasmale-
mma 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). Not-
withstanding 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 under-
standing 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 trans-
port in higher plants.
Active transport of silicic acid in rice
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 trans-
port, 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.
Where now?
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 en-
hanced 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 import-
ant 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
www.newphytologist.com © New Phytologist (2003) 158: 419 – 430

ocean (Ajtay et al., 1979; Falkowski & Raven, 1997; Field
et al., 1998).
John A. Raven
Division of Environmental and Applied Biology,
School of Life Sciences
University of Dundee, Dundee DD1 4HN, UK
(tel +44 1382344281; fax +44 1382344275;
email j.a.raven@dundee.ac.uk)
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Commentary Forum 421
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Key words: silicon, active transport, diatoms, grasses, rice, silica,
silicic acid, weathering.
Commentary
158
Woody plants, carbon
allocation and fine roots
Sitting on the veranda, the sun reflects off the Mosel and
the long rows of Vitis vinifera sloping down to the river.
It’s a lazy autumn afternoon and my mind drifts from the
nuances of the Embden-Meyerhof-Parnas pathway to the
beautiful, neatly manicured rows of grape vines. The leaves
are pale yellow and the physiological processes preceding
the advent of the dormant season are unfolding. These
vines are highly integrated physiological systems, with water,
minerals, amino acids, carbohydrates, growth regulators,
and other organic substances moving freely, though often in
phases, between roots and shoots. How old are these vines?
How deeply rooted are they, perched on this dry, south-
facing slope? The ability of woody plants to survive for
decades, centuries, sometimes millennia, is due in part to
their capacity to withstand environmental stress by shifting
their resources from roots, to shoots, to storage reserves.
Grapes are no exception – vines can be in production for
decades, and they survive the year-to-year vagaries of nature
and horticultural manipulations designed to encourage higher
berry yields by shifting resource allocation. In this issue of
New Phytologist (pp. 489–501), Anderson et al. report
how irrigation, pruning and annual variations in weather
influence the survivorship of roots of Concord grape, Vitus
labruscana. There are two interesting perspectives raised:
• The importance of whole plant source–sink relationships
in driving fine root lifespan.
• Fine roots as modular plant organs with different life
expectancies depending on various environmental and
developmental factors.