Annals of Botany 101: 463–468, 2008
doi:10.1093/aob/mcm301, available online at www.aob.oxfordjournals.org
Relationships Between Photosynthetic Activity and Silica Accumulation
with Ages of Leaf in Sasa veitchii (Poaceae, Bambusoideae)
H IROYU KI MOTOMU RA 1,2 , * , KOU KI HI KO S AK A 3 and M I T S U O S U Z U K I 1
1
The Botanical Garden of Tohoku University, Aoba-ku, Sendai 980-0862, Japan, 2Environmental Stress Research Unit,
National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan and 3Graduate School of Science,
Tohoku University, Aoba-ku, Sendai 980-8578, Japan
Received: 10 September 2007 Returned for revision: 17 October 2007 Accepted: 2 November 2007 Published electronically: 27 November 2007
† Background and Aims Bamboos have long-lived, evergreen leaves that continue to accumulate silica throughout
their life. Silica accumulation has been suggested to suppress their photosynthetic activity. However, nitrogen
content per unit leaf area (Narea), an important determinant of maximum photosynthetic capacity per unit leaf
area (Pmax), decreases as leaves age and senescence. In many species, Pmax decreases in parallel with the leaf nitrogen content. It is hypothesized that if silica accumulation affects photosynthesis, then Pmax would decrease faster
than Narea, leading to a decrease in photosynthetic rate per unit leaf nitrogen ( photosynthetic nitrogen use efficiency,
PNUE) with increasing silica content in leaves.
† Methods The hypothesis was tested in leaves of Sasa veitchii, which have a life span of 2 years and accumulate
silica up to 41 % of dry mass. Seasonal changes in Pmax, stomatal conductance, Narea and silica content were
measured for leaves of different ages.
† Key Results Although Pmax and PNUE were negatively related with silica content across leaves of different ages,
the relationship between PNUE and silica differed depending on leaf age. In second-year leaves, PNUE was almost
constant although there was a large increase in silica content, suggesting that leaf nitrogen was a primary factor
determining the variation in Pmax and that silica accumulation did not affect photosynthesis. PNUE was strongly
and negatively correlated with silica content in third-year leaves, suggesting that silica accumulation affected photosynthesis of older leaves.
† Conclusions Silica accumulation in long-lived leaves of bamboo did not affect photosynthesis when the silica concentration of a leaf was less than 25 % of dry mass. Silica may be actively transported to epidermal cells rather than
chlorenchyma cells, avoiding inhibition of CO2 diffusion from the intercellular space to chloroplasts. However, in
older leaves with a larger silica content, silica was also deposited in chlorenchyma cells, which may relate to the
decrease in PNUE.
Key words: Sasa veitchii, bamboo, leaf, silica accumulation, photosynthetic capacity, nitrogen content, photosynthetic
nitrogen use efficiency, leaf age, leaf senescence.
IN TROD UCT IO N
Silica accumulation is an important characteristic of plants
belonging to the family Poaceae. Silicon in the form of
silicic acid is absorbed from the soil, and mainly accumulated in the aerial parts as amorphous hydrated silica
(SiO2.nH2O). Various functions have been proposed for
silica accumulation, such as mechanical stability of
tissues, protection against fungi, insects and herbivores,
resistance to drought, facilitation of light interception, and
alleviation of problems caused by nutrient deficiency and
excess (Jones and Handreck, 1967; Raven, 1983; Sangster
and Hodson, 1986; Marschner, 1995; Prychid et al., 2003;
Richmond and Sussman, 2003; Epstein and Bloom, 2005;
Fauteux et al., 2005; Hattori et al., 2005; Ma and Yamaji,
2006).
Within the Poaceae, bamboos deposit silica in mature
leaves in variable but generally large concentrations (2–
41 % SiO2 on a dry mass basis; Ueda and Ueda, 1961;
Yamane and Sato, 1971; Takahashi et al., 1981; Kaneko,
1995; Motomura et al., 2000, 2002). Leaves of
Phyllostachys pubescens and P. bambusoides live for 1
* For correspondence. E-mail [email protected]
year, and their silica concentration increases rapidly in the
early growing season of the first year, levels-off in the
first autumn, and then increases slightly or does not
change in the early spring of the following year (Ueda
and Ueda, 1961; Kaneko, 1995). Leaves of Sasa veitchii,
which have a life span of 2 years, accumulate silica not
only during expansion in early development, but also
after maturation until defoliation in the summer and
autumn of the third year (Motomura et al., 2002).
Motomura et al. (2002) showed that the changes in silica
content depended on the season, and the accumulation
pattern (rapid in summer and slow in spring and winter)
was repeated during the 2 years of the life span.
Transpiration may affect silica accumulation processes,
as water flow in the transpiration stream brings silica dissolved in water from the roots to the leaves. Silica is deposited along conductive tissues and heavy deposition is often
observed at the end of the transpiration stream, for example
in leaf tips and inflorescence bracts (Frey-Wyssling, 1930;
Ueda and Ueda, 1961; Yoshida et al., 1962; Jones and
Handreck, 1967; Handreck and Jones, 1968; Takahashi
and Miyake, 1976). The hypothesis that silica deposition
is determined only by transpiration explains why rapid
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464
Motomura et al. — Photosynthesis and Silica in Sasa Leaves
silica accumulation in bamboo leaves is greatest in summer,
when water loss is greatest as stomatal pores are open and
photosynthesis occurs. Another hypothesis regarding the
relationship between silica and the physiological activity
of leaves has been suggested (Ellis, 1979; Motomura
et al., 2000), namely that silica deposition inhibits photosynthesis in the leaf. The consequences of silica deposition
on leaf function have not been clarified. Silica is deposited
more in the chlorenchyma cells of older leaves than those of
young leaves (Sangster, 1970; Motomura et al., 2000),
which may prevent CO2 diffusion from the intercellular
space to chloroplasts. Experiments on rice (Oryza sativa)
in hydroponic solutions with different silica concentrations
have shown that silica accumulation in leaves does not
reduce photosynthetic activity (Kawamitsu et al., 1989;
Agarie et al., 1992a,b). However, the rice leaves used in
these studies have smaller silica concentrations (less than
18 % SiO2 on a dry mass basis) than those in bamboos.
To test the hypothesis that silica accumulation inhibits
photosynthesis, we examined the relationship between
silica accumulation and photosynthetic activity in bamboo
leaves with large silica contents during their life cycle.
Photosynthetic capacity (Pmax; see Table 1 for a list of
abbreviations) changes with many aspects of leaf development and physiology (e.g. age of leaf, and protein composition and amount) and not only with silica content. Leaf
nitrogen, which largely reflects the protein content, is a
primary factor for the variation of Pmax in the leaves, particularly because a large amount of nitrogen is invested in
the photosynthetic apparatus (Field and Mooney, 1986;
Evans, 1989; Hikosaka, 2004). As leaves age, Pmax
decreases as photosynthetic proteins are degraded and the
nitrogen is translocated to other tissues. In many species,
Pmax decreases in parallel with decreasing nitrogen
content per area (Narea) with an almost constant photosynthetic rate per unit leaf nitrogen ( photosynthetic nitrogen
use efficiency, PNUE; Reich et al., 1991; Karlsson, 1994;
Miyazawa et al., 2005; Yasumura et al., 2006). However,
in some other species Pmax decreases faster than Narea,
leading to a decrease in PNUE with leaf age (Wilson
et al., 2000; Kitajima et al., 2002; Escudero and
Mediavilla, 2003; Miyazawa et al., 2004). In these
species, the age-dependent change in Pmax is caused not
only by leaf nitrogen but also by other factors.
We hypothesize that silica accumulation may affect the
Pmax/Narea relationship. Since silica content increases with
leaf age, if silica accumulation suppresses CO2 diffusion
in leaves and thus inhibits photosynthesis, Pmax should
TA B L E 1. Abbreviations used in the text
gs
Stomatal conductance to water vapour
LMA
Leaf mass per unit leaf area
LMASF
Leaf mass per unit leaf area without silica
Narea
Nitrogen content per unit leaf area
Pmax
Photosynthetic rate
PNUE
Photosynthetic nitrogen use efficiency
SiO2 area
Silica content per unit leaf area
decrease faster than Narea, leading to a decrease in PNUE
with increasing silica content. We assessed PNUE in the
leaves of Sasa veitchii, which have a longer leaf life span
(2 years) than other bamboos in which the consequences
of silica accumulation has been studied. They accumulate
silica up to 41 % on a dry mass basis, the largest recorded
silica concentration in higher plants (Motomura et al.,
2002). In this study, photosynthetic characteristics, including PNUE, were determined periodically together with
silica deposition in leaves of different leaf ages and the
relationships between them were analysed.
M AT E R I A L S A N D M E T H O D S
Sasa veitchii (Carrière) Rehder was studied. The population
was under trees (Abies firma, Acer mono, Hovenia dulcis,
Neolitsea sericea, Populus sieboldii and Prunus buergeriana) growing in the Botanical Garden of Tohoku
University, Sendai, Japan, in an old-growth, temperate
mixed forest near the northern limit of this vegetation
zone. The canopy of the deciduous trees began to develop
in mid-May and leaves were shed in mid- and
late-November. The mean annual temperature was 11.9 8C
with a total precipitation of 1440 mm (Sugawara, 1969;
Kurosawa et al., 1995).
Ninety-nine fully expanded leaves were examined from
April to December in 2000: their silica contents have
been reported previously (Motomura et al., 2002). In Sasa
veitchii, new culm branches appear sympodially from the
nodes every year, and each branch has leaves similar to
those of the top of older branches. In April 2000, leaves
that emerged in different years (1998 and 1999) were distinguished on the basis of the branching pattern related to the
sequence of the emergence of culm branches. Each branch
that emerged in 1998 had leaves on the second, third or
fourth nodes from the top of the branches, and these
remaining leaves were shed during summer and autumn
in 2000. In June 2000, current-year branches that appeared
from the basal part of older branches that had emerged in
1999 had several leaves of different developmental stages,
and fully expanded leaves appeared on several nodes of
the top of the branches before all the leaves finished to
unfold in August (see Figs 1 and 2 of Motomura et al.
2002). In this study, fully expanded leaves from each
branch that emerged in three different years (2000, 1999
and 1998) were distinguished as three age classes, i.e.
first-, second- and third-year leaves, respectively.
Seasonal changes in gas exchange characteristics,
maximum rate of net photosynthesis (Pmax), transpiration
rate and stomatal conductance (gs) were determined with
a portable photosynthesis system (LI-6400P, Li-Cor Inc.,
NE, USA). At each time point, we used a leaf from each
of three to five branches that had emerged in three different
years. Environmental conditions in the chamber were regulated to give a photon flux of 1000 mmol quanta m22 s21,
a leaf temperature of 25 + 1 8C, CO2 concentration of
375– 400 mL L21 and a vapour pressure deficit of less
than 1 KPa. The measurements were done twice on two
sunny days for each leaf.
Motomura et al. — Photosynthesis and Silica in Sasa Leaves
465
F I G . 1. Seasonal changes in (A) silica content per unit leaf area (SiO2 area), (B) leaf dry mass minus silica content per unit leaf area (LMASF), (C) leaf
mass per unit leaf area (LMA), (D) stomatal conductance to water vapor (gs), (E) light-saturated photosynthetic rate (Pmax), (F) nitrogen content per unit
leaf area (Narea), and (G) photosynthetic nitrogen use efficiency (PNUE) in leaves of Sasa veitchii of three different ages. Bars indicate s.e.
After the gas exchange measurements, the leaves were
collected, washed with distilled water, cut into three equal
sections (basal, middle and top), and discs were punched
out from the median part between the leaf margin and
midrib of the middle sections: three discs of 2.4 cm2 for
determination of nitrogen content and one disc of 3.1 cm2
466
Motomura et al. — Photosynthesis and Silica in Sasa Leaves
F I G . 2. Relationships between (A) light-saturated photosynthetic rate
(Pmax) and (B) photosynthetic nitrogen use efficiency (PNUE), and silica
content on a unit area basis (SiO2 area) in leaves of Sasa veitchii at three
different ages.
for determination of dry mass and silica content. The discs
were weighed after drying for 48 h at 80 8C. Nitrogen
content was determined with an NC analyzer (NC-80,
Sumitomo Chemical Co., Tokyo, Japan). Silica content
was determined photometrically by colorimetric reaction
using the molybdenum blue method (Motomura et al.,
2002). To analyse the relationship between silica accumulation and leaf photosynthetic characteristics, the accumulation rate of silica was calculated as: [SiO2 area of the
current month – SiO2 area of the previous month] for each
period, where SiO2 area is the silica content per unit leaf
area. We also calculated the potential transpiration rate as
the product of stomatal conductance and maximum daily
vapour pressure deficit (VPDmax), the latter being calculated from the maximum daily air temperature and relative
humidity determined at the Botanical Garden.
Simple correlation analyses between silica accumulation
and photosynthetic characteristics were carried out with gs,
Narea, Pmax, PNUE, SiO2 area and silica accumulation rate as
independent variables using JMP version 5 (SAS Institute
Inc., NC, USA).
R E S U LT S
The silica content per unit leaf area (SiO2 area), increased
rapidly in spring and summer in leaves of all ages
(Fig. 1A), as did silica concentration per dry mass: 3 – 15,
15– 25 and 25– 41 % for first-, second- and third-year
leaves, respectively (see Motomura et al., 2002).
Silica-free leaf mass per unit area (LMASF) increased only
in spring and summer in first-year leaves and was constant
in second- and third-year leaves (Fig. 1B). Total leaf mass
per unit area (LMA) increased with leaf age (Fig. 1C).
Stomatal conductance (gs) in first- and second-year
leaves increased markedly from spring to summer, and
then decreased rapidly towards the end of the growing
season; however, it was almost constant in third-year
leaves (Fig. 1D). Photosynthetic capacity (Pmax) in firstyear leaves increased gradually from spring until midsummer, and then decreased slightly (Fig. 1E). Pmax in
second and third-year leaves was highest in spring, and
decreased gradually in summer; it became stable at the
end of the growing season in all ages of leaves. Nitrogen
content per unit area (Narea) in first-year leaves increased
gradually towards the end of the growing season, but in
second- and third-year leaves it was greatest in spring and
winter, and smallest in summer (Fig. 1F).
Photosynthetic nitrogen efficiency (PNUE), calculated as
the ratio of Pmax : Narea, showed a large difference between
the three leaf age classes (Fig. 1G). It was highest in the
spring in first-year leaves and rapidly decreased through
to winter. Second-year leaves had constant PNUE throughout the season. Third-year leaves had similar PNUE to
second-year leaves in early spring, but then it gradually
decreased until death.
Pmax was negatively correlated with SiO2 area across the
three age classes (Table 2). However, the correlation
between Pmax and SiO2 area was positive if data of first-year
leaves only were considered, and was negative if data for
second- and third-year leaves only were considered
(Fig. 2A). PNUE was also negatively correlated with
SiO2 area (Table 2). However, the regression again varied
among the leaf age classes (Fig. 2B); PNUE decreased
TA B L E 2. Correlation coefficients (r) and significance levels
(P) for measured parameters in leaves of Sasa veitchii at
three different ages. See Table 1 for abbreviations
PNUE vs. gs
Pmax vs. gs
Narea vs. gs
Narea vs. Pmax
LMASF vs. gs
LMASF vs. PNUE
LMASF vs. Pmax
LMASF vs. Narea
SiO2 area vs. gs
SiO2 area vs. PNUE
SiO2 area vs. Pmax
SiO2 area vs. Narea
SiO2 area vs. LMASF
Silica accumulation rate vs. gs
Silica accumulation rate vs. PNUE
Silica accumulation rate vs. Pmax
Silica accumulation rate vs. Narea
Silica accumulation rate vs. LMASF
Silica accumulation rate vs. SiO2 area
n
r
P
18
25
18
18
18
18
18
18
18
18
18
18
21
15
15
15
15
18
18
0.6304
0.4073
–0.5422
0.3353
–0.5294
–0.8513
–0.3456
0.7781
–0.4869
–0.8931
–0.8725
0.0852
0.6835
0.0983
–0.2130
–0.1840
0.1271
0.3731
0.3098
0.0050
0.0433
0.0201
0.1738
0.0239
0.0000
0.1601
0.0001
0.0405
0.0000
0.0000
0.7367
0.0006
0.7274
0.4460
0.5115
0.6518
0.1272
0.2109
Motomura et al. — Photosynthesis and Silica in Sasa Leaves
with increasing SiO2 area in first- and third-year leaves,
whereas it was constant in second-year leaves. It should
be noted that there was no decrease in PNUE between 8 –
16 g m22 of SiO2 area.
There was no significant correlation between the silica
accumulation rate and other leaf characteristics (Table 2):
the accumulation rate correlated neither with the transpiration rate determined when Pmax was obtained, nor with the
potential transpiration rate (gs VPDmax; P . 0.05, data
not shown).
DISCUSSION
We tested the hypothesis that silica accumulation suppressed photosynthesis. If silica simply accumulates in
leaf tissues without negative effects on photosynthesis,
then there would be no effects on Pmax or Narea, and so
no correlation between them and SiO2 area. If silica accumulation has a direct effect on some essential process in leaf
physiology, then there would be a strong, negative correlation. In leaves of Sasa veitchii, Pmax was negatively correlated with the silica content (Fig. 2A). However, Pmax
in first-year leaves increased with increasing silica content
(Fig. 2A), and Pmax was similar between first-year leaves
in winter and third-year leaves in spring (Fig. 1E),
showing that Pmax was unaffected by silica content, which
was considerably different between the two. Furthermore,
Pmax in the second-year leaves of S. veitchii showed a
similar seasonal change to that in Narea, so PNUE remained
constant when silica content increased from 8 to 16 g m22
(Fig. 2B), suggesting that Pmax was mainly regulated by
nitrogen investment in the leaves irrespective of silica
accumulation. Based on these observations, we conclude
that the silica content is not a primary factor for the variation of Pmax in first- and second-year leaves of S. veitchii.
This is consistent with previous studies showing that
silica accumulation did not negatively affect Pmax in rice
leaves in a range up to 18 % silica concentration
(Kawamitsu et al., 1989; Agarie et al., 1992a,b).
However, in third-year leaves of S. veitchii, which had
very large silica concentrations (more than 25 % on a dry
mass basis), Pmax decreased more rapidly than Narea,
leading to a large decrease in PNUE (Fig. 1E, G).
Consequently, PNUE was strongly correlated with the
silica content (Fig. 2B). Thus, we hypothesize that silica
accumulation affects photosynthesis only in third-year
leaves. Most silica accumulation was found in epidermal
cells in leaves of S. veitchii and there was no silica deposition in chlorenchyma cells in first- and second-year
leaves (Motomura et al., 2004). However, it was found
that third-year leaves accumulated silica also in chlorenchyma cells (see figs 1 and 4 in Motomura et al., 2004).
As CO2 is transferred through the surface of chlorenchyma
cells, silica deposition might reduce CO2 diffusion from the
intercellular space to the chloroplasts. These results suggest
that silica deposition has negative effects on photosynthesis
if the silica concentration is higher than 25 % on a leaf dry
mass basis. However, an age-dependent decrease in PNUE
has been observed in some species with less silica accumulation (Wilson et al., 2000; Kitajima et al., 2002; Escudero
467
and Mediavilla, 2003; Miyazawa et al., 2004). Niinemets
et al. (2005) showed that the CO2 partial pressure in chloroplasts decreased with leaf age in several Mediterranean
evergreen, broadleaved species. Thus, further study is
needed to assess whether silica deposition inhibits CO2 diffusion in chlorenchyma cells.
Transpiration has been considered to affect the silica
accumulation process (Frey-Wyssling, 1930; Yoshida
et al., 1962; Frey-Wyssling and Mühlethaler, 1965;
Handreck and Jones, 1968; Aston and Jones, 1976;
Kaufman et al., 1981; Jarvis, 1987; Walker and Lance,
1991). If transpiration has a direct effect on the silica
accumulation process in leaves, then there would be a
strong correlation between Pmax or stomatal conductance
(gs) and the silica accumulation rate. In leaves of
S. veitchii, however, the silica accumulation rate was not
correlated with CO2 exchange or gs (Table 2). Thus, silica
accumulation must be associated with factors other than
transpiration. Silica may be accumulated depending on
plant demand, because silica uptake rate in some grass
species does not depend on the water absorption (Barber
and Shone, 1966; Vorm, 1980; Jarvis, 1987; Walker and
Lance, 1991), suggesting that the silica is taken up in an
active rather than in a passive manner. Sasa veitchii
leaves tend to be damaged by herbivores in spring and
summer (H. Motomura, pers. obs.); rapid, selective
accumulation of silica in summer (Motomura et al., 2004)
may serve to decrease herbivory.
In summary, silica accumulation in leaves of bamboo did
not affect photosynthesis, at least when the silica concentration of a leaf was less than 25 % on a dry mass basis.
Plants may actively transport silica to epidermal cells
rather than to chlorenchyma cells that actively photosynthesize, so avoiding inhibition of CO2 diffusion from the intercellular space to the chloroplasts. However, in ageing leaves
with a greater silica content, silica was deposited in chlorenchyma cells as well, which may relate to the decrease
in PNUE.
AC KN OW L E DG E M E N T S
We thank Drs Osamu Ueno (National Institute of
Agrobiological Sciences, Japan), Tomoyuki Fujii and
Yuko Yasumura (Forestry and Forest Products Research
Institute, Japan) for helpful comments on an early draft of
the manuscript, Sakae Agarie (Saga University, Japan) for
valuable advice, David Lawlor for critically reviewing the
manuscript prior to publication, and Mr Takahiro Tsukui
(Botanical Garden of Tohoku University, Japan) for information on meteorological data.
L IT E RAT URE C IT E D
Agarie S, Agata W, Kubota F, Kaufman PB. 1992a. Physiological roles
of silicon in photosynthesis and dry matter production in rice
plants. I. Effects of silicon and shading treatments. Japanese
Journal of Crop Science 61: 200–206 (in Japanese).
Agarie S, Uchida H, Agata W, Kubota F. 1992b. Varietal difference in
effects of silicon application on photosynthesis and dry matter production in rice plants. Science Bulletin of the Faculty of
Agriculture, Kyushu University 47: 7– 16 (in Japanese).
468
Motomura et al. — Photosynthesis and Silica in Sasa Leaves
Aston MM, Jones MM. 1976. A study of the transpiration surfaces of
Avena sterilis L. var. Algerian leaves using monosilicic acid as a
tracer for water movement. Planta 130: 121– 129.
Barber DA, Shone MG. 1966. The absorption of silica from aqueous solutions by plants. Journal of Experimental Botany 17: 569– 578.
Ellis RP. 1979. A procedure for standardizing comparative leaf anatomy in
the Poaceae. II. The epidermis as seen in surface view. Bothalia 12:
641–671.
Epstein E, Bloom AJ. 2005. Mineral nutrition of plants, 2nd edn.
Sunderland, MA: Sinauer Associates.
Escudero A, Mediavilla S. 2003. Decline in photosynthetic nitrogen use
efficiency with leaf age and nitrogen resorption as determinants of
leaf life span. Journal of Ecology 91: 880– 889.
Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3
plants. Oecologia 78: 9– 19.
Fauteux F, Remus-Borel W, Menzies JG, Belanger RR. 2005. Silicon
and plant disease resistance against pathogenic fungi. FEMS
Microbiology Letters 249: 1– 9.
Field C, Mooney H. 1986. The photosynthesis–nitrogen relationship in
wild plants. In: Givnish TJ, ed. On the economy of form and function.
Cambridge: Cambrige University Press, 22– 55.
Frey-Wyssling A. 1930. Vergleich zwischen der ausscheidung von kieselsäure und kalziumsalzen in der pflanze. Berichte der Deutschen
Botanischen Gesellschaft 48: 184– 191.
Frey-Wyssling A, Mühlethaler K. 1965. Ultrastructural plant cytology.
Amsterdam: Elsevier Publishing Company.
Handreck KA, Jones LHP. 1968. Studies of silica in the oat plant. IV.
Silica content of plant parts in relation to stage of growth, supply of
silica, and transpiration. Plant and Soil 24: 449– 459.
Hattori T, An P, Inanaga S. 2005. Effects of silicon application on
drought tolerance of crops. Root Research 14: 41–49 (in Japanese).
Hikosaka K. 2004. Interspecific difference in the photosynthesis– nitrogen
relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research 117: 481–494.
Jarvis SC. 1987. The uptake and transport of silicon by perennial ryegrass
and wheat. Plant and Soil 97: 429– 437.
Jones LHP, Handreck KA. 1967. Silica in soils, plants, and animals.
Advances in Agronomy 19: 107– 149.
Kaneko S. 1995. Seasonal change of nutrient concentrations in
Phyllostachys bambusoides and Phyllostachys pubescens. Bamboo
Journal 13: 27– 33 (in Japanese).
Karlsson PS. 1994. Photosynthetic capacity and photosynthetic
nutrient-use efficiency of Rhododendron lapponicum leaves as
related to leaf nutrient status, leaf age and branch reproductive
status. Functional Ecology 8: 694– 700.
Kaufman PB, Dayanandan P, Takeoka Y, Bigelow WC, Jones JD, Iler
R. 1981. Silica in shoots of higher plants. In: Simpson TL, Volcani
BE, eds. Silicon and siliceous structures in biological systems.
New York: Springer, 409–449.
Kawamitsu M, Kawamitsu Y, Agata W, Kaufman PB. 1989. Effect of
SiO2 on CO2 assimilation rate, transpiration rate, leaf conductance
and dry matter production in rice plants. Science Bulletin of the
Faculty of Agriculture, Kyushu University 43: 161–169 (in Japanese).
Kitajima K, Mulkey SS, Samaniego M, Wright SJ. 2002. Decline of
photosynthetic capacity with leaf age and position in two tropical
pioneer tree species. American Journal of Botany 89: 1925– 1932.
Kurosawa T, Tateishi Y, Kajita T. 1995. Flora of Aobayama, wild vascular plants in the botanical garden of Tohoku University, Japan.
Ecological Review 23: 111–170.
Ma JF, Yamaji N. 2006. Silicon uptake and accumulation in higher plants.
Trends in Plant Science 11: 392–397.
Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. San
Diego: Academic Press.
Miyazawa S-I, Suzuki AA, Sone K, Terashima I. 2004. Relationships
between light, leaf nitrogen and nitrogen remobilization in the
crowns of mature evergreen Quercus glauca trees. Tree Physiology
24: 1157–1164.
Miyazawa SI, Satomi S, Terashima I. 2005. Winter photosynthesis by
saplings of evergreen broad-leaved trees in a deciduous temperate
forest. New Phytologist 165: 857–866.
Motomura H, Fujii T, Suzuki M. 2000. Distribution of silicified cells in
the leaf blades of Pleioblastus chino (Franchet et Savatier) Makino
(Bambusoideae). Annals of Botany 85: 751– 757.
Motomura H, Mita N, Suzuki M. 2002. Silica accumulation in long-lived
leaves of Sasa veitchii (Carriére) Rehder (Poaceae–Bambusoideae).
Annals of Botany 90: 149– 152.
Motomura H, Fujii T, Suzuki M. 2004. Silica deposition in relation to
ageing of leaf tissues in Sasa veitchii (Carriére) Rehder (Poaceae:
Bambusoideae). Annals of Botany 93: 235– 248.
Niinemets U, Cescatti A, Rodeghiero M, Tosens T. 2005. Leaf internal
diffusion conductance limits photsynthesis more strongly in older
leaves of Mediterranean evergreen broad-leaved species. Plant, Cell
and Environment 28: 1552–1566.
Prychid CJ, Rudall PJ, Gregory M. 2003. Systematics and biology of
silica bodies in monocotyledons. Botanical Review 69: 377 –440.
Raven JA. 1983. The transport and function of silicon in plants. Biological
Review 58: 179– 207.
Reich PB, Walters MB, Ellsworth DS. 1991. Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and
photosynthesis in maple and oak trees. Plant, Cell and Environment
14: 251– 259.
Richmond KE, Sussman M. 2003. Got silicon? The non-essential beneficial plant nutrient. Current Opinion in Plant Biology 6: 268– 272.
Sangster AG. 1970. Intracellular silica deposition in mature and senescent
leaves of Sieglingia decumbens (L.) Bernh. Annals of Botany 34:
559–570.
Sangster AG, Hodson MJ. 1986. Silica in higher plants. In: Evered D,
O’Connor M, eds. Silicon biochemistry. Chichester, UK: Wiley,
90–111.
Sugawara K. 1969. Ecological studies in the botanical garden of the
Tohoku University. I. Present state of vegetation. Ecological Review
17: 111– 127.
Takahashi E, Miyake Y. 1976. Silica content in plants among organs and
growth stage. Journal of the Science of Soil and Manure, Japan 47:
338–341 (in Japanese).
Takahashi E, Tanaka T, Miyake Y. 1981. Distribution of silicicolous
plant in plant kingdom (5). Journal of the Science of Soil and
Manure, Japan 52: 503– 510 (in Japanese).
Ueda K, Ueda S. 1961. Effect of silicic acid on bamboo-growth. Bulletin
of the Kyoto University Forests 33: 79–99 (in Japanese).
Vorm PDJ. 1980. Uptake of Si by five plant species, as influenced by variations in Si-supply. Plant and Soil 56: 153–156.
Walker CD, Lance RCM. 1991. Silicon accumulation and 13C composition as indices of water-use efficiency in barley cultivars.
Australian Journal of Plant Physiology 18: 427–434.
Wilson KB, Baldocchi DD, Hanson PJ. 2000. Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiology 20: 565–578.
Yamane I, Sato K. 1971. Seasonal change of chemical composition in
Sasa palmata. Report of the Institute for Agricultural Research,
Tohoku University 22: 37–66.
Yasumura S, Hikosaka K, Hirose T. 2006. Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera
umbellata leaves grown in high or low irradiance. Tree Physiology
26: 1315–1323.
Yoshida S, Ohnishi Y, Kitagishi K. 1962. Histochemistry of silicon in
plants II. Localization of silicon within rice tissues. Soil Science
and Plant Nutrition 8: 36– 41.