Вы находитесь на странице: 1из 6

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
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,

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010
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 nitro-
gen 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 photo-
synthesis of older leaves.
† Conclusions Silica accumulation in long-lived leaves of bamboo did not affect photosynthesis when the silica con-
centration 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 year, and their silica concentration increases rapidly in the
early growing season of the first year, levels-off in the
Silica accumulation is an important characteristic of plants
first autumn, and then increases slightly or does not
belonging to the family Poaceae. Silicon in the form of
change in the early spring of the following year (Ueda
silicic acid is absorbed from the soil, and mainly accumu-
and Ueda, 1961; Kaneko, 1995). Leaves of Sasa veitchii,
lated in the aerial parts as amorphous hydrated silica
which have a life span of 2 years, accumulate silica not
(SiO2.nH2O). Various functions have been proposed for
only during expansion in early development, but also
silica accumulation, such as mechanical stability of
after maturation until defoliation in the summer and
tissues, protection against fungi, insects and herbivores,
autumn of the third year (Motomura et al., 2002).
resistance to drought, facilitation of light interception, and
Motomura et al. (2002) showed that the changes in silica
alleviation of problems caused by nutrient deficiency and
content depended on the season, and the accumulation
excess (Jones and Handreck, 1967; Raven, 1983; Sangster
pattern (rapid in summer and slow in spring and winter)
and Hodson, 1986; Marschner, 1995; Prychid et al., 2003;
was repeated during the 2 years of the life span.
Richmond and Sussman, 2003; Epstein and Bloom, 2005;
Transpiration may affect silica accumulation processes,
Fauteux et al., 2005; Hattori et al., 2005; Ma and Yamaji,
as water flow in the transpiration stream brings silica dis-
solved in water from the roots to the leaves. Silica is depos-
Within the Poaceae, bamboos deposit silica in mature
ited along conductive tissues and heavy deposition is often
leaves in variable but generally large concentrations (2–
observed at the end of the transpiration stream, for example
41 % SiO2 on a dry mass basis; Ueda and Ueda, 1961;
in leaf tips and inflorescence bracts (Frey-Wyssling, 1930;
Yamane and Sato, 1971; Takahashi et al., 1981; Kaneko,
Ueda and Ueda, 1961; Yoshida et al., 1962; Jones and
1995; Motomura et al., 2000, 2002). Leaves of
Handreck, 1967; Handreck and Jones, 1968; Takahashi
Phyllostachys pubescens and P. bambusoides live for 1
and Miyake, 1976). The hypothesis that silica deposition
* For correspondence. E-mail hmochi@affrc.go.jp is determined only by transpiration explains why rapid
# The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: journals.permissions@oxfordjournals.org
464 Motomura et al. — Photosynthesis and Silica in Sasa Leaves

silica accumulation in bamboo leaves is greatest in summer, decrease faster than Narea, leading to a decrease in PNUE
when water loss is greatest as stomatal pores are open and with increasing silica content. We assessed PNUE in the
photosynthesis occurs. Another hypothesis regarding the leaves of Sasa veitchii, which have a longer leaf life span
relationship between silica and the physiological activity (2 years) than other bamboos in which the consequences
of leaves has been suggested (Ellis, 1979; Motomura of silica accumulation has been studied. They accumulate
et al., 2000), namely that silica deposition inhibits photo- silica up to 41 % on a dry mass basis, the largest recorded
synthesis in the leaf. The consequences of silica deposition silica concentration in higher plants (Motomura et al.,
on leaf function have not been clarified. Silica is deposited 2002). In this study, photosynthetic characteristics, includ-
more in the chlorenchyma cells of older leaves than those of ing PNUE, were determined periodically together with

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010
young leaves (Sangster, 1970; Motomura et al., 2000), silica deposition in leaves of different leaf ages and the
which may prevent CO2 diffusion from the intercellular relationships between them were analysed.
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 Sasa veitchii (Carrière) Rehder was studied. The population
these studies have smaller silica concentrations (less than was under trees (Abies firma, Acer mono, Hovenia dulcis,
18 % SiO2 on a dry mass basis) than those in bamboos. Neolitsea sericea, Populus sieboldii and Prunus buergeri-
To test the hypothesis that silica accumulation inhibits ana) growing in the Botanical Garden of Tohoku
photosynthesis, we examined the relationship between University, Sendai, Japan, in an old-growth, temperate
silica accumulation and photosynthetic activity in bamboo mixed forest near the northern limit of this vegetation
leaves with large silica contents during their life cycle. zone. The canopy of the deciduous trees began to develop
Photosynthetic capacity (Pmax; see Table 1 for a list of in mid-May and leaves were shed in mid- and
abbreviations) changes with many aspects of leaf develop- late-November. The mean annual temperature was 11.9 8C
ment and physiology (e.g. age of leaf, and protein compo- with a total precipitation of 1440 mm (Sugawara, 1969;
sition and amount) and not only with silica content. Leaf Kurosawa et al., 1995).
nitrogen, which largely reflects the protein content, is a Ninety-nine fully expanded leaves were examined from
primary factor for the variation of Pmax in the leaves, par- April to December in 2000: their silica contents have
ticularly because a large amount of nitrogen is invested in been reported previously (Motomura et al., 2002). In Sasa
the photosynthetic apparatus (Field and Mooney, 1986; veitchii, new culm branches appear sympodially from the
Evans, 1989; Hikosaka, 2004). As leaves age, Pmax nodes every year, and each branch has leaves similar to
decreases as photosynthetic proteins are degraded and the those of the top of older branches. In April 2000, leaves
nitrogen is translocated to other tissues. In many species, that emerged in different years (1998 and 1999) were distin-
Pmax decreases in parallel with decreasing nitrogen guished on the basis of the branching pattern related to the
content per area (Narea) with an almost constant photosyn- sequence of the emergence of culm branches. Each branch
thetic rate per unit leaf nitrogen ( photosynthetic nitrogen that emerged in 1998 had leaves on the second, third or
use efficiency, PNUE; Reich et al., 1991; Karlsson, 1994; fourth nodes from the top of the branches, and these
Miyazawa et al., 2005; Yasumura et al., 2006). However, remaining leaves were shed during summer and autumn
in some other species Pmax decreases faster than Narea, in 2000. In June 2000, current-year branches that appeared
leading to a decrease in PNUE with leaf age (Wilson from the basal part of older branches that had emerged in
et al., 2000; Kitajima et al., 2002; Escudero and 1999 had several leaves of different developmental stages,
Mediavilla, 2003; Miyazawa et al., 2004). In these and fully expanded leaves appeared on several nodes of
species, the age-dependent change in Pmax is caused not the top of the branches before all the leaves finished to
only by leaf nitrogen but also by other factors. unfold in August (see Figs 1 and 2 of Motomura et al.
We hypothesize that silica accumulation may affect the 2002). In this study, fully expanded leaves from each
Pmax/Narea relationship. Since silica content increases with branch that emerged in three different years (2000, 1999
leaf age, if silica accumulation suppresses CO2 diffusion and 1998) were distinguished as three age classes, i.e.
in leaves and thus inhibits photosynthesis, Pmax should first-, second- and third-year leaves, respectively.
Seasonal changes in gas exchange characteristics,
TA B L E 1. Abbreviations used in the text maximum rate of net photosynthesis (Pmax), transpiration
rate and stomatal conductance (gs) were determined with
gs Stomatal conductance to water vapour a portable photosynthesis system (LI-6400P, Li-Cor Inc.,
LMA Leaf mass per unit leaf area NE, USA). At each time point, we used a leaf from each
LMASF Leaf mass per unit leaf area without silica of three to five branches that had emerged in three different
Narea Nitrogen content per unit leaf area
years. Environmental conditions in the chamber were regu-
lated to give a photon flux of 1000 mmol quanta m22 s21,
Pmax Photosynthetic rate
a leaf temperature of 25 + 1 8C, CO2 concentration of
PNUE Photosynthetic nitrogen use efficiency 375– 400 mL L21 and a vapour pressure deficit of less
SiO2 area Silica content per unit leaf area 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

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010

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 out from the median part between the leaf margin and
collected, washed with distilled water, cut into three equal midrib of the middle sections: three discs of 2.4 cm2 for
sections (basal, middle and top), and discs were punched determination of nitrogen content and one disc of 3.1 cm2
466 Motomura et al. — Photosynthesis and Silica in Sasa Leaves

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

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010
season; however, it was almost constant in third-year
leaves (Fig. 1D). Photosynthetic capacity (Pmax) in first-
year leaves increased gradually from spring until mid-
summer, 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 through-
out the season. Third-year leaves had similar PNUE to
second-year leaves in early spring, but then it gradually
decreased until death.
F I G . 2. Relationships between (A) light-saturated photosynthetic rate Pmax was negatively correlated with SiO2 area across the
(Pmax) and (B) photosynthetic nitrogen use efficiency (PNUE), and silica three age classes (Table 2). However, the correlation
content on a unit area basis (SiO2 area) in leaves of Sasa veitchii at three
different ages. 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
for determination of dry mass and silica content. The discs (Fig. 2A). PNUE was also negatively correlated with
were weighed after drying for 48 h at 80 8C. Nitrogen SiO2 area (Table 2). However, the regression again varied
content was determined with an NC analyzer (NC-80, among the leaf age classes (Fig. 2B); PNUE decreased
Sumitomo Chemical Co., Tokyo, Japan). Silica content
was determined photometrically by colorimetric reaction
using the molybdenum blue method (Motomura et al., TA B L E 2. Correlation coefficients (r) and significance levels
2002). To analyse the relationship between silica accumu- (P) for measured parameters in leaves of Sasa veitchii at
lation and leaf photosynthetic characteristics, the accumu- three different ages. See Table 1 for abbreviations
lation rate of silica was calculated as: [SiO2 area of the
current month – SiO2 area of the previous month] for each n r P
period, where SiO2 area is the silica content per unit leaf
area. We also calculated the potential transpiration rate as PNUE vs. gs 18 0.6304 0.0050
the product of stomatal conductance and maximum daily Pmax vs. gs 25 0.4073 0.0433
Narea vs. gs 18 –0.5422 0.0201
vapour pressure deficit (VPDmax), the latter being calcu- Narea vs. Pmax 18 0.3353 0.1738
lated from the maximum daily air temperature and relative LMASF vs. gs 18 –0.5294 0.0239
humidity determined at the Botanical Garden. LMASF vs. PNUE 18 –0.8513 0.0000
Simple correlation analyses between silica accumulation LMASF vs. Pmax 18 –0.3456 0.1601
and photosynthetic characteristics were carried out with gs, LMASF vs. Narea 18 0.7781 0.0001
SiO2 area vs. gs 18 –0.4869 0.0405
Narea, Pmax, PNUE, SiO2 area and silica accumulation rate as SiO2 area vs. PNUE 18 –0.8931 0.0000
independent variables using JMP version 5 (SAS Institute SiO2 area vs. Pmax 18 –0.8725 0.0000
Inc., NC, USA). SiO2 area vs. Narea 18 0.0852 0.7367
SiO2 area vs. LMASF 21 0.6835 0.0006
Silica accumulation rate vs. gs 15 0.0983 0.7274
R E S U LT S Silica accumulation rate vs. PNUE 15 –0.2130 0.4460
Silica accumulation rate vs. Pmax 15 –0.1840 0.5115
The silica content per unit leaf area (SiO2 area), increased Silica accumulation rate vs. Narea 15 0.1271 0.6518
Silica accumulation rate vs. LMASF 18 0.3731 0.1272
rapidly in spring and summer in leaves of all ages Silica accumulation rate vs. SiO2 area 18 0.3098 0.2109
(Fig. 1A), as did silica concentration per dry mass: 3 – 15,
Motomura et al. — Photosynthesis and Silica in Sasa Leaves 467

with increasing SiO2 area in first- and third-year leaves, and Mediavilla, 2003; Miyazawa et al., 2004). Niinemets
whereas it was constant in second-year leaves. It should et al. (2005) showed that the CO2 partial pressure in chlor-
be noted that there was no decrease in PNUE between 8 – oplasts decreased with leaf age in several Mediterranean
16 g m22 of SiO2 area. evergreen, broadleaved species. Thus, further study is
There was no significant correlation between the silica needed to assess whether silica deposition inhibits CO2 dif-
accumulation rate and other leaf characteristics (Table 2): fusion in chlorenchyma cells.
the accumulation rate correlated neither with the transpira- Transpiration has been considered to affect the silica
tion rate determined when Pmax was obtained, nor with the accumulation process (Frey-Wyssling, 1930; Yoshida
potential transpiration rate (gs  VPDmax; P . 0.05, data et al., 1962; Frey-Wyssling and Mühlethaler, 1965;

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010
not shown). 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
We tested the hypothesis that silica accumulation sup- strong correlation between Pmax or stomatal conductance
pressed photosynthesis. If silica simply accumulates in (gs) and the silica accumulation rate. In leaves of
leaf tissues without negative effects on photosynthesis, S. veitchii, however, the silica accumulation rate was not
then there would be no effects on Pmax or Narea, and so correlated with CO2 exchange or gs (Table 2). Thus, silica
no correlation between them and SiO2 area. If silica accumu- accumulation must be associated with factors other than
lation has a direct effect on some essential process in leaf transpiration. Silica may be accumulated depending on
physiology, then there would be a strong, negative corre- plant demand, because silica uptake rate in some grass
lation. In leaves of Sasa veitchii, Pmax was negatively cor- species does not depend on the water absorption (Barber
related with the silica content (Fig. 2A). However, Pmax and Shone, 1966; Vorm, 1980; Jarvis, 1987; Walker and
in first-year leaves increased with increasing silica content Lance, 1991), suggesting that the silica is taken up in an
(Fig. 2A), and Pmax was similar between first-year leaves active rather than in a passive manner. Sasa veitchii
in winter and third-year leaves in spring (Fig. 1E), leaves tend to be damaged by herbivores in spring and
showing that Pmax was unaffected by silica content, which summer (H. Motomura, pers. obs.); rapid, selective
was considerably different between the two. Furthermore, accumulation of silica in summer (Motomura et al., 2004)
Pmax in the second-year leaves of S. veitchii showed a may serve to decrease herbivory.
similar seasonal change to that in Narea, so PNUE remained In summary, silica accumulation in leaves of bamboo did
constant when silica content increased from 8 to 16 g m22 not affect photosynthesis, at least when the silica concen-
(Fig. 2B), suggesting that Pmax was mainly regulated by tration of a leaf was less than 25 % on a dry mass basis.
nitrogen investment in the leaves irrespective of silica Plants may actively transport silica to epidermal cells
accumulation. Based on these observations, we conclude rather than to chlorenchyma cells that actively photosynthe-
that the silica content is not a primary factor for the varia- size, so avoiding inhibition of CO2 diffusion from the inter-
tion of Pmax in first- and second-year leaves of S. veitchii. cellular space to the chloroplasts. However, in ageing leaves
This is consistent with previous studies showing that with a greater silica content, silica was deposited in chlor-
silica accumulation did not negatively affect Pmax in rice enchyma cells as well, which may relate to the decrease
leaves in a range up to 18 % silica concentration in PNUE.
(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 AC KN OW L E DG E M E N T S
mass basis), Pmax decreased more rapidly than Narea, We thank Drs Osamu Ueno (National Institute of
leading to a large decrease in PNUE (Fig. 1E, G). Agrobiological Sciences, Japan), Tomoyuki Fujii and
Consequently, PNUE was strongly correlated with the Yuko Yasumura (Forestry and Forest Products Research
silica content (Fig. 2B). Thus, we hypothesize that silica Institute, Japan) for helpful comments on an early draft of
accumulation affects photosynthesis only in third-year the manuscript, Sakae Agarie (Saga University, Japan) for
leaves. Most silica accumulation was found in epidermal valuable advice, David Lawlor for critically reviewing the
cells in leaves of S. veitchii and there was no silica depo- manuscript prior to publication, and Mr Takahiro Tsukui
sition in chlorenchyma cells in first- and second-year (Botanical Garden of Tohoku University, Japan) for infor-
leaves (Motomura et al., 2004). However, it was found mation on meteorological data.
that third-year leaves accumulated silica also in chloren-
chyma cells (see figs 1 and 4 in Motomura et al., 2004).
As CO2 is transferred through the surface of chlorenchyma L IT E RAT URE C IT E D
cells, silica deposition might reduce CO2 diffusion from the Agarie S, Agata W, Kubota F, Kaufman PB. 1992a. Physiological roles
intercellular space to the chloroplasts. These results suggest of silicon in photosynthesis and dry matter production in rice
that silica deposition has negative effects on photosynthesis plants. I. Effects of silicon and shading treatments. Japanese
if the silica concentration is higher than 25 % on a leaf dry Journal of Crop Science 61: 200–206 (in Japanese).
Agarie S, Uchida H, Agata W, Kubota F. 1992b. Varietal difference in
mass basis. However, an age-dependent decrease in PNUE effects of silicon application on photosynthesis and dry matter pro-
has been observed in some species with less silica accumu- duction in rice plants. Science Bulletin of the Faculty of
lation (Wilson et al., 2000; Kitajima et al., 2002; Escudero 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 crowns of mature evergreen Quercus glauca trees. Tree Physiology
Avena sterilis L. var. Algerian leaves using monosilicic acid as a 24: 1157–1164.
tracer for water movement. Planta 130: 121– 129. Miyazawa SI, Satomi S, Terashima I. 2005. Winter photosynthesis by
Barber DA, Shone MG. 1966. The absorption of silica from aqueous sol- saplings of evergreen broad-leaved trees in a deciduous temperate
utions by plants. Journal of Experimental Botany 17: 569– 578. forest. New Phytologist 165: 857–866.
Ellis RP. 1979. A procedure for standardizing comparative leaf anatomy in Motomura H, Fujii T, Suzuki M. 2000. Distribution of silicified cells in
the Poaceae. II. The epidermis as seen in surface view. Bothalia 12: the leaf blades of Pleioblastus chino (Franchet et Savatier) Makino
641–671. (Bambusoideae). Annals of Botany 85: 751– 757.
Epstein E, Bloom AJ. 2005. Mineral nutrition of plants, 2nd edn. Motomura H, Mita N, Suzuki M. 2002. Silica accumulation in long-lived
Sunderland, MA: Sinauer Associates. leaves of Sasa veitchii (Carriére) Rehder (Poaceae–Bambusoideae).
Escudero A, Mediavilla S. 2003. Decline in photosynthetic nitrogen use Annals of Botany 90: 149– 152.

Downloaded from http://aob.oxfordjournals.org at Universiti Teknologi MARA - Shah Alam on August 17, 2010
efficiency with leaf age and nitrogen resorption as determinants of Motomura H, Fujii T, Suzuki M. 2004. Silica deposition in relation to
leaf life span. Journal of Ecology 91: 880– 889. ageing of leaf tissues in Sasa veitchii (Carriére) Rehder (Poaceae:
Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3 Bambusoideae). Annals of Botany 93: 235– 248.
plants. Oecologia 78: 9– 19.
Niinemets U, Cescatti A, Rodeghiero M, Tosens T. 2005. Leaf internal
Fauteux F, Remus-Borel W, Menzies JG, Belanger RR. 2005. Silicon
diffusion conductance limits photsynthesis more strongly in older
and plant disease resistance against pathogenic fungi. FEMS
leaves of Mediterranean evergreen broad-leaved species. Plant, Cell
Microbiology Letters 249: 1– 9.
and Environment 28: 1552–1566.
Field C, Mooney H. 1986. The photosynthesis–nitrogen relationship in
wild plants. In: Givnish TJ, ed. On the economy of form and function. Prychid CJ, Rudall PJ, Gregory M. 2003. Systematics and biology of
Cambridge: Cambrige University Press, 22– 55. silica bodies in monocotyledons. Botanical Review 69: 377 –440.
Frey-Wyssling A. 1930. Vergleich zwischen der ausscheidung von kiesel- Raven JA. 1983. The transport and function of silicon in plants. Biological
säure und kalziumsalzen in der pflanze. Berichte der Deutschen Review 58: 179– 207.
Botanischen Gesellschaft 48: 184– 191. Reich PB, Walters MB, Ellsworth DS. 1991. Leaf age and season influ-
Frey-Wyssling A, Mühlethaler K. 1965. Ultrastructural plant cytology. ence the relationships between leaf nitrogen, leaf mass per area and
Amsterdam: Elsevier Publishing Company. photosynthesis in maple and oak trees. Plant, Cell and Environment
Handreck KA, Jones LHP. 1968. Studies of silica in the oat plant. IV. 14: 251– 259.
Silica content of plant parts in relation to stage of growth, supply of Richmond KE, Sussman M. 2003. Got silicon? The non-essential bene-
silica, and transpiration. Plant and Soil 24: 449– 459. ficial plant nutrient. Current Opinion in Plant Biology 6: 268– 272.
Hattori T, An P, Inanaga S. 2005. Effects of silicon application on Sangster AG. 1970. Intracellular silica deposition in mature and senescent
drought tolerance of crops. Root Research 14: 41–49 (in Japanese). leaves of Sieglingia decumbens (L.) Bernh. Annals of Botany 34:
Hikosaka K. 2004. Interspecific difference in the photosynthesis– nitrogen 559–570.
relationship: patterns, physiological causes, and ecological impor- Sangster AG, Hodson MJ. 1986. Silica in higher plants. In: Evered D,
tance. Journal of Plant Research 117: 481–494. O’Connor M, eds. Silicon biochemistry. Chichester, UK: Wiley,
Jarvis SC. 1987. The uptake and transport of silicon by perennial ryegrass 90–111.
and wheat. Plant and Soil 97: 429– 437. Sugawara K. 1969. Ecological studies in the botanical garden of the
Jones LHP, Handreck KA. 1967. Silica in soils, plants, and animals. Tohoku University. I. Present state of vegetation. Ecological Review
Advances in Agronomy 19: 107– 149. 17: 111– 127.
Kaneko S. 1995. Seasonal change of nutrient concentrations in Takahashi E, Miyake Y. 1976. Silica content in plants among organs and
Phyllostachys bambusoides and Phyllostachys pubescens. Bamboo growth stage. Journal of the Science of Soil and Manure, Japan 47:
Journal 13: 27– 33 (in Japanese). 338–341 (in Japanese).
Karlsson PS. 1994. Photosynthetic capacity and photosynthetic Takahashi E, Tanaka T, Miyake Y. 1981. Distribution of silicicolous
nutrient-use efficiency of Rhododendron lapponicum leaves as plant in plant kingdom (5). Journal of the Science of Soil and
related to leaf nutrient status, leaf age and branch reproductive Manure, Japan 52: 503– 510 (in Japanese).
status. Functional Ecology 8: 694– 700. Ueda K, Ueda S. 1961. Effect of silicic acid on bamboo-growth. Bulletin
Kaufman PB, Dayanandan P, Takeoka Y, Bigelow WC, Jones JD, Iler of the Kyoto University Forests 33: 79–99 (in Japanese).
R. 1981. Silica in shoots of higher plants. In: Simpson TL, Volcani
Vorm PDJ. 1980. Uptake of Si by five plant species, as influenced by vari-
BE, eds. Silicon and siliceous structures in biological systems.
ations in Si-supply. Plant and Soil 56: 153–156.
New York: Springer, 409–449.
Walker CD, Lance RCM. 1991. Silicon accumulation and 13C compo-
Kawamitsu M, Kawamitsu Y, Agata W, Kaufman PB. 1989. Effect of
SiO2 on CO2 assimilation rate, transpiration rate, leaf conductance sition as indices of water-use efficiency in barley cultivars.
and dry matter production in rice plants. Science Bulletin of the Australian Journal of Plant Physiology 18: 427–434.
Faculty of Agriculture, Kyushu University 43: 161–169 (in Japanese). Wilson KB, Baldocchi DD, Hanson PJ. 2000. Spatial and seasonal varia-
Kitajima K, Mulkey SS, Samaniego M, Wright SJ. 2002. Decline of bility of photosynthetic parameters and their relationship to leaf nitro-
photosynthetic capacity with leaf age and position in two tropical gen in a deciduous forest. Tree Physiology 20: 565–578.
pioneer tree species. American Journal of Botany 89: 1925– 1932. Yamane I, Sato K. 1971. Seasonal change of chemical composition in
Kurosawa T, Tateishi Y, Kajita T. 1995. Flora of Aobayama, wild vascu- Sasa palmata. Report of the Institute for Agricultural Research,
lar plants in the botanical garden of Tohoku University, Japan. Tohoku University 22: 37–66.
Ecological Review 23: 111–170. Yasumura S, Hikosaka K, Hirose T. 2006. Seasonal changes in photo-
Ma JF, Yamaji N. 2006. Silicon uptake and accumulation in higher plants. synthesis, nitrogen content and nitrogen partitioning in Lindera
Trends in Plant Science 11: 392–397. umbellata leaves grown in high or low irradiance. Tree Physiology
Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. San 26: 1315–1323.
Diego: Academic Press. Yoshida S, Ohnishi Y, Kitagishi K. 1962. Histochemistry of silicon in
Miyazawa S-I, Suzuki AA, Sone K, Terashima I. 2004. Relationships plants II. Localization of silicon within rice tissues. Soil Science
between light, leaf nitrogen and nitrogen remobilization in the and Plant Nutrition 8: 36– 41.