Physiological and Ecological Significance of Biomineralization in Plants

Review

Physiological and ecological signiﬁcance of biomineralization

1,2,3 3 4 3

Honghua He , Erik J. Veneklaas , John Kuo , and Hans Lambers

State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation,

Northwest A&F University, Yangling, Shaanxi 712100, China

Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling,

Shaanxi 712100, China

School of Plant Biology, The University of Western Australia, Crawley (Perth), WA 6009, Australia

Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley (Perth), WA 6009, Australia

Biomineralization is widespread in the plant kingdom. stress, regulating ion balance (e.g., sodium and potassium),

The most common types of biominerals in plants are detoxifying oxalic acid, disposing of alkalinity generated by

calcium oxalate crystals, calcium carbonate, and silica. nitrate assimilation in above-ground organs, protecting

Functions of biominerals may depend on their shape, plants against herbivory and pathogen attack, providing

size, abundance, placement, and chemical composition. tissue rigidity and mechanical support, and guiding posi-

In this review we highlight advances in understanding tively gravitropic growth of the rhizoids of charophycean

physiological and ecological signiﬁcance of biominerali- algae [1–3,13,17,19,23,29–32].

zation in plants. We focus on the functions of biominer-

alization in regulating cytoplasmic free calcium levels,

detoxifying aluminum and heavy metals, light gathering

and scattering to optimize photosynthesis, aiding in Glossary

pollen release, germination, and tube growth, the roles

Biogeochemical cycle: a circuit or pathway by which a chemical element or

it plays in herbivore deterrence, biogeochemical cycling molecule moves through both biotic and abiotic compartments of an

ecosystem. While all elements are recycled, in some such cycles there

of carbon, calcium, and silicon, and sequestering atmo-

may be sinks where the elements are accumulated or held for a long period

spheric CO2. of time.

Biomineralization: the process by which organisms form minerals. The

formation of biominerals may be ‘biologically induced’ or ‘biologically

Biomineralization in plants

controlled’ ‘biologically controlled’ is also termed ‘matrix-mediated’. In

Biomineralization (see Glossary) occurs in most organs and

‘biologically induced’ mineralization the organism modifies its proximal

tissues within plants [1–4]. Commonly reported biomin- environment and creates physicochemical conditions favoring mineral pre-

cipitation; the process is promoted by the organism but the organism has little

erals in plants are calcium oxalate (CaOX) crystals [5–8],

or no control over the localization, orientation, morphology, or composition of

calcium carbonate (amorphous CaCO3 or calcite) [9–11], the crystals, and no specific biomolecules or organic matrices are involved in

and amorphous silica [12–14]. Calcium sulfate [15–18], the processes. By contrast, in’ biologically controlled’ mineralization the

localization, nucleation, growth, shape, and size of crystals are controlled by

calcium phosphate [19], magnesium oxalate [15,20,21],

the organism, and organic matrices made up of proteins, polysaccharides,

strontium oxalate [20,22], and strontium and barium sul- proteolipids, and proteoglycans produced by the organism are responsible for

the control.

fate [16,20,23] have been observed in some plant species.

Coccolithophores: a group of unicellular marine phytoplankton which produce

Metals such as sodium, potassium, aluminum, iron, man-

minute calcite plates, termed coccoliths, around each living cell as an outer

ganese, cadmium, and zinc are also found in biominerals in covering or scales. Coccoliths are typical ‘biologically controlled’ biominerals.

Cryo-SEM-EDX: Cryo-scanning energy-dispersive X-ray microanalysis, a

some plants [10,20,24–28], indicating that the chemical

technique used to determine the distribution and concentration of elements

composition of biominerals in plants is diverse.

in situ at the level of individual cells and sometimes within cell organelles, in

There are several hypotheses to the functions of biomin- which bulk tissues are rapidly frozen in liquid nitrogen (termed cryo-fixation),

water and soluble compounds are preserved, and the shapes and dimensions

eralization in plants, including regulating cytoplasmic

of hydrated structures are retained in situ from life to examination in the SEM.

calcium levels, detoxifying aluminum and heavy metals,

Cystolith: amorphous calcium carbonate in plants.

gathering and scattering light, aiding in pollen release and Druse: a crystal conglomerate that is thought to be formed by precipitation of

multiple crystals around a nucleation site.

germination, alleviating water, salt, and temperature

EDX: energy-dispersive X-ray microanalysis.

Frustule: the hard and porous cell wall or external layer of diatoms, which is

composed of very pure hydrated silica.

Corresponding author: He, H. ([email protected]).

Phyllodes: modified petioles that function as leaves.

1360-1385/$ – see front matter Phytolith: usually refers to amorphous silica formed in plants, also termed

all biominerals in plants.

SEM: scanning electron microscopy.

Thiophore: a plant with a leaf sulfur concentration ranging from 25 to

–1

82 mg S g dry weight.

166 Trends in Plant Science, March 2014, Vol. 19, No. 3

Review Trends in Plant Science March 2014, Vol. 19, No. 3

In addition to the above-proposed physiological func- for example duckweed (Lemna minor) [6], common bean

tions, biomineralization in plants is also of ecological (Phaseolus vulgaris) [2,41], mulberry (Morus australis [42],

signiﬁcance [33] and it is this aspect that we will focus and Jew’s mallow (Corchorus olitorius), the production of

on in this review. In fact, a ﬁeld of research on the role CaOX crystals increases with increasing calcium concen-

plants play in biogeochemical cycles via biomineralization tration in the growth medium, indicating that the forma-

has been developed, including the study of carbon, calci- tion of CaOX crystals as calcium sinks is inducible [43].

um, and silicon ﬂuxes [34–36]. Here we highlight the There is also evidence that the formation of CaOX is a rapid

physiological signiﬁcance of biomineralization in calcium and reversible process. Calcium stored in CaOX can be

regulation, detoxiﬁcation of aluminum and heavy metals, remobilized under conditions when calcium is limiting to

light regulation, and facilitating pollen release, germina- plant growth and development [42,44,45]; in such cases

tion, and tube growth, as well as its ecological signiﬁcance CaOX crystals act as calcium reserves. However, there are

in herbivore deterrence and biogeochemical cycling of examples showing that CaOX formation in some tissues

carbon, calcium, and silicon, and sequestering of atmo- and/or plants is not inducible by changes in soil calcium

spheric CO2. availability [46,47]. To explain the different responses

between tissues and/or plants requires studies on the

Physiological signiﬁcance molecular mechanisms underlying calcium regulation

Calcium regulation and oxalate synthesis.

Calcium is an essential plant nutrient with many funda- The formation of CaCO3 is another component of

mental functions in cellular metabolism [37]. In most calcium metabolism; for example, in leaves of mulberry

plants cytoplasmic free calcium required for cellular me- the size of individual amorphous CaCO3 depositions

–7

tabolism is maintained at 10 M or less. Plants often increases with increasing calcium concentration in the

accumulate calcium in excess of cytoplasmic requirements. growth medium. However, the formation of CaCO3 may

Excessive free calcium in the cytoplasm is toxic to plants play a less-important role in calcium regulation than

and interferes with several metabolic processes, including CaOX does in mulberry leaves because its formation is

calcium-dependent signaling and phosphate-based energy less responsive to changes in calcium supply [42]. It is

metabolism; therefore cytoplasmic free calcium levels are necessary to study the formation of CaOX and CaCO3 in

tightly controlled [4]. response to calcium supply in a comparative way on

Sequestering excessive calcium in a physiologically and more plant species to clarify which of the two types of

osmotically inactive form is an effective way to regulate calcium biominerals is more closely linked with calcium

cytoplasmic free calcium levels and avoiding potential toxic regulation.

effects. Calcium oxalate crystals are the most common Other types of calcium biominerals such as calcium

types of biominerals in plants; they account for 3À80% sulfate may also play an important role in calcium regu-

of plant dry weight and up to 90% of the total calcium of a lation in certain plants; for example, robe’s wattle (Aca-

plant, and calcium regulation is one of the most important cia robeorum) native to the Great Sandy Desert in north-

proposed functions of CaOX [2]. Relative to surrounding western Australia has a large amount of calcium sulfate

mesophyll cells, crystal idioblasts of water lettuce (Pistia crystals in its phyllodes (Figure 1) and branchlets [15].

stratiotes) act as high-capacity calcium sinks, accumulat- Concentrations of calcium, magnesium, and sulfur in the

–1

ing large amounts of calcium within the vacuole as CaOX phyllodes of robe’s wattle are 72, 10, and 42 mg g (dry

crystals [38]. Deposition of CaOX in cells in the vicinity of weight), respectively [15]; this species can be identiﬁed as

the stomatal guard cells is responsible for the necessary a thiophore [48]. The sulfur and magnesium crystals

calcium regulation, and may contribute to the effective may serve as sulfur and magnesium sinks, and regulate

stomatal control of gas exchange [39,40]. In some plants, sulfur and magnesium levels in the cytoplasm (Figure 2).

(A) (B) (C) (D)

TRENDS in Plant Science

Figure 1. Phyllodes (arrowed) of (A) Acacia robeorum, (B) Acacia ancistrocarpa, (C) Acacia stipuligera, and (D) Acacia stellaticeps. All scale bars are equivalent to 2 cm.

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(A) (F)

C Ca

0 1 2 3 4 5 (B)(B ) (C)(C) keV (G) Ca

(D) C O K

0 1 2 3 4 5 keV (H)

(E) Mg Ca

0 1 2 3 4 5 keV (I) Ca

C O Ca

Mg S

0 1 2 3 4 5 keV

TRENDS in Plant Science

Figure 2. Abundant oxalate and sulfate biominerals of calcium (Ca) and magnesium (Mg) in phyllodes of Acacia robeorum. (A–E) Scanning electron microscopy (SEM)

images. (F–I) Energy-dispersive X-ray microanalysis (EDX) spectra of biominerals. (A) A view of a whole cross-section of a phyllode with an abundance of biominerals. (B)

An enlarged view of the area within the white rectangle in panel (A), showing amorphous and/or druse biominerals (filled arrow) and spherical biominerals (unfilled arrow).

(C) A cluster of amorphous and/or druse biominerals. (D) Part of a cross section of a phyllode showing a large amount of amorphous and/or druse biominerals and raphides

(arrow head). (E) A cross-sectional view of a half of a phyllode filled with raphides. (F,G) Spectra of amorphous and/or druse biominerals. (H) Spectrum of spherical

biominerals. (I) Spectrum of raphides. Scale bars: (A), 200 mm; (B), 100 mm; (C), 20 mm; (D), 10 mm; (E), 50 mm. Adapted from [15].

Biogenic formation of calcium sulfate crystals may Detoxiﬁcation of aluminum and heavy metals

also explain the high foliar calcium and sulfur concen- Several studies show involvement of CaOX crystals in

trations of a few other Acacia species in north-western aluminum and heavy-metal detoxiﬁcation. Incorporation

Australia (P. Hayes, B. Turner, H. Lambers, E. Laliberte´, of aluminum into CaOX crystals has been observed in

unpublished). leaves of Jew’s mallow [49]. The presence of strontium

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in CaOX crystals has been documented in leaves of duck- CaOX crystals in leaves of water hyacinth [50] and in

weed, sugar beet (Beta vulgaris), pink fringe (Arthrostema various tissues of tomato (Solanum lycopersicum) [51].

ciliatum), and silky glycine (Glycine canescens) [22]; in Crystallization of CaOX may also play a role in lead (Pb)

leaves of water hyacinth (Eichhornia crassipes) [50]; in deposition and tolerance in leaves of water hyacinth [50].

phyllodes and branchlets of Fitzroy wattle (Acacia ancis- However, addition of heavy metals such as zinc and lead

trocarpa) [20], and in phyllodes of Acacia stipuligera and decreases the number of CaOX crystals, without inclusion

robe’s wattle (Figure 3). Cadmium has been detected in of heavy metals in CaOX crystals in leaves of common

bean, suggesting that CaOX crystals do not play a major

role in heavy-metal detoxiﬁcation of this heavy-metal sen-

(A) (E)

sitive species [52]. The results of the above-mentioned

Ca studies indicate that deposition of heavy metals in CaOX

crystals is both metal- and plant species-speciﬁc.

Intracellular sequestration of heavy metals such as man-

ganese, zinc, and strontium with CaCO3 has been reported

in leaves of Cuban laurel (Ficus retusa) [10]. In tobacco

(Nicotiana tabacum&rpar) plants, excretion of cadmium-

C and/or zinc-substituted CaCO3 grains and other zinc-con-

Sr Ca

taining compounds (e.g., zinc organic compounds, zinc-

sorbed silica, and zinc-sorbed phosphate) via trichomes is

0 1 2 3 4 5 6

keV regarded a potent detoxiﬁcation mechanism [28,53,54].

(B) (F) S In many plants silicon is mainly incorporated into the

Ca cell walls, and coprecipitation of aluminum and heavy

metals with silicon in the cell walls may be responsible

for the alleviation of their toxicity. Such alleviation of

toxicity has been demonstrated by the formation of alumi-

num silicate in epidermal cell walls of sorghum (Sorghum

bicolor) [55], white spruce (Picea glauca) [56], and maize

(Zea mays) [57]. In leaves of bladder campion (Silene

Ca vulgaris ssp. humilis), a heavy-metal-tolerant plant grow-

C Sr

ing on the polluted soil of a medieval copper-mining dump,

0 1 2 3 4 5 6

keV zinc and tin accumulated in cell walls as silicate [58].

showed a decreased percentage and concentration of sym-

S plasmic manganese, and an increased percentage and

concentration of manganese bound to the leaf cell walls,

resulting in higher manganese tolerance [59]. Simulta-

neous presence of silica, cadmium, and zinc deposits has

Ba been observed in cell walls of epidermis, exodermis, and

C endodermis of maize roots [60]. Codeposition of aluminum

CaBa Ba and heavy metals with silica can signiﬁcantly reduce the

O K Ca Ba

Ba apoplasmic transport of these metals, thus alleviating

0 1 2 3 4 5 6 their toxic effects on plants [55,60]. Coprecipitation of

keV

heavy metals and silicon can also occur in the symplasm;

(D) (H) for example, when Arabidopsis (formerly Cardaminopsis)

halleri, a zinc- and cadmium-hyperaccumulator, is grown

on a zinc- and copper-polluted soil, zinc coprecipitates with

S silicon and forms zinc silicate in the cytoplasm and nuclei

of leaf cells, and the formation of zinc silicate is regarded as

part of the zinc-tolerance mechanism of this species [61].

Ba Cadmium and zinc coprecipitate with silicon in the cyto-

C Ca plasm and vacuoles of mesophyll cells when maize is grown

K Ba Ba O Ca on a cadmium- and zinc-enriched soil [60]. In phyllodes of

BaBa

A. stipuligera and robe’s wattle, coprecipitation of alumi-

0 1 2 3 4 5 6

keV num and iron with silicon has been observed (Figure 4).

There are other mechanisms involved in silicon-mediated

TRENDS in Plant Science

aluminum and heavy-metal detoxiﬁcation in higher plants;

Figure 3. Sequestration of strontium (Sr) and barium (Ba) in oxalate and sulfate

these are summarized in earlier reviews [62,63].

biominerals formed in phyllodes of four Acacia species. (A–D) Scanning electron

microscopy (SEM) images of biominerals (arrow) in phyllodes of Acacia Beyond CaOX, CaCO3, and silica, there are other types

ancistrocarpa, Acacia robeorum, Acacia stipuligera, and Acacia stellaticeps, of biominerals that may contribute to heavy-metal detoxi-

respectively. (E–H) Corresponding energy-dispersive X-ray microanalysis (EDX)

ﬁcation in plants. In charophycean algae such as desmids

spectra of biominerals in (A–D). Scale bars: (A), 5 mm; (B), 10 mm; (C, D), 2 mm.

Adapted from [20]. and Charales the formation of strontium and barium

169

Review Trends in Plant Science March 2014, Vol. 19, No. 3 (A) (D)

C O

Si Au Fe Al

K Ca Fe Au Ca Fe 0 1 2 3 4 5 6 7 8 9 10 keV (B) (E)

S Ca

O Au

C Fe Si Ca

Fe Fe Au 0 1 2 3 4 5 6 7 8 9 10 keV

C Mn O Au Mn

Cu Au Mn Cu Au CaCa Cu 0 1 2 3 4 5 6 7 8 9 10 keV

TRENDS in Plant Science

Figure 4. Sequestration of aluminum (Al), iron (Fe), manganese (Mn), and copper (Cu) in silicate and sulfate biominerals formed in phyllodes of two Acacia species.

(A) Scanning electron microscopy (SEM) image of a biomineral (arrow) in a phyllode of Acacia stipuligera; (B,C) SEM images of biominerals (arrow) in phyllodes of Acacia

robeorum. (D–F) Corresponding energy-dispersive X-ray microanalysis (EDX) spectra of biominerals in (A–C). Scale bars: (A,B), 2.5 mm; (C), 1 mm.

sulfates is relatively common [23], even in the presence of Light regulation

an excess of calcium [16]. The desmid green alga (Closter- Light gathering and reﬂection is one of the proposed func-

ium moniliferum) is effective in remediating Sr and tions of CaOX druse crystals [2,64]. In leaves of six Pepero-

cleaning nuclear waste [16]. Formation of sulfate biomin- mia species, which are low-light-adapted, CaOX druse

erals may play a role in detoxifying heavy metals such as crystals are speciﬁcally produced in the photosynthetic

strontium, barium, manganese, and copper in land plants, palisade cells rather than in specialized idioblasts, and

for example in A. stipuligera, glistening wattle (Acacia each palisade cell contains a druse crystal within its vacu-

stellaticeps) [20], and robe’s wattle (Figures 3 and 4). ole, indicating that the crystals play a role other than

It remains unclear to what degree biomineralization calcium regulation in these plants [65]. In cypress pepero-

contributes to aluminum and heavy-metal detoxiﬁcation. mia (Peperomia glabella) the size of druse crystals in

The detoxiﬁcation mechanisms are expected to be eluci- palisade cells decreases with increasing light intensity.

dated by studying the anatomy, physiology, and molecular The position of the crystals also changes with light inten-

biology of the plants in combination, using modern tech- sity, showing that the crystals move up as the light inten-

nologies such as Cryo-SEM-EDX to localize aluminum, sity increases. It is hypothesized that the crystals help to

heavy metals and biominerals in plants, identifying key distribute light evenly to the chloroplasts. Placing the

genes controlling biomineralization, heavy-metal uptake crystals at the middle or bottom of the cells at low light

and detoxiﬁcation, and establishing correlations between levels would help distribute the limited light to the chlor-

expression of these genes and toxicity of aluminum and oplasts towards the bottom half of the palisade cells and

heavy metals. Isotope/pulse–chase techniques may also be maximize light capture; at high light levels crystals formed

applied to quantify metal ions as a function of time and at the top of the palisade cells may dissipate excess light by

spatial distribution within plant tissues and/or cells. reﬂecting part of the light back up to the window tissue,

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thus protecting the shade-adapted chloroplasts from by insects as well as large animals, and this function is

photodamage and minimizing photoinhibition [65,66]. Fur- achieved either physically or chemically depending on the

ther support for this hypothesis comes from a study that shape, size, placement, abundance, and chemical composi-

demonstrated that the refractive indices of cystoliths and tion of the biominerals [1–3,72].

CaOX druses in leaves of small-fruited ﬁg (Ficus micro- For a Negev desert lily (Pancratium sickenbergeri), only

carpa) are signiﬁcantly higher than those of the surround- the leaf parts devoid of CaOX raphide crystals are con-

ing cytoplasm and cell wall, thus the cystoliths and CaOX sumed by dorcas gazelle; comparisons of the abundance of

druses act as light scatterers and reduce the steep light CaOX raphides in different lily populations revealed that

gradient generated by photosynthetic pigments, enabling the severity of herbivory in different populations correlates

the leaf to use the incoming light ﬂux more efﬁciently [67]. negatively with their raphide abundance [46]. In leaves of

The authors also found that the spatial distribution of the arrow-leaf sida (Sida rhombifolia) subjected to herbivory

biominerals is compatible with their optical function. The [73], CaOX production increases, indicating that formation

above-mentioned results suggest that biominerals are in- of CaOX crystals in some tissues and/or plants is an

volved in the photosynthetic process in land plants [66,67]. inducible defense response to herbivory. However, it is

Coccoliths are effective at scattering light, making a suggested that the formation of CaOX crystals in some

coccolithophore bloom easily visible from space by satellite tissues and/or plants is a constitutive rather than induced

[11]. There is much debate about the role of coccoliths in defense against herbivores. For example, after simulated

light scattering in coccolithophores. The optical signature herbivory by clipping bulbs [74] and leaves [47] of the

of coccolithophore blooms is largely (80%) a result of the Negev desert lily, the number of CaOX crystals did not

detached coccoliths that are freely ﬂoating, rather than the increase signiﬁcantly. In some conifer species, increased

living cells themselves [68]. Whether light scattering by CaOX crystal accumulation in the secondary phloem

biominerals is common and functionally important in the appears to be antagonistic to beetle attack, suggesting

plant kingdom warrants further critical study. that CaOX crystals functions as a constitutive defense

against small bark-boring insects [75]. Constitutive de-

Facilitating pollen release, germination, and tube fense may well be a more appropriate strategy than in-

growth duced defense in environments with unpredictability,

Calcium oxalate crystals may facilitate pollen release and especially when leaves are ephemeral and herbivore pres-

germination. In anthers of chili pepper (Capsicum sure is high [47].

annuum) there are many CaOX crystals in the connective The deposition of solid hydrated amorphous silica rein-

tissue and in the hypodermal stomium between adjacent forces the cell wall and protects many plants against

locules. It has been suggested that calcium is systemati- attacks by herbivores through increasing the abrasiveness

cally removed from the cytoplasm and cell walls of the and reducing the digestibility of plant tissues [1,76–78].

connective tissue and the stomium, and is sequestered in Plants native to heavily-grazed habitats accumulate more

CaOX crystals when the pollen matures. This leads to silica than plants native to less-heavily-grazed habitats,

degradation and weakening of the cell walls between the and plants attacked by herbivores accumulate more silica

locules, followed by collapse of the connective tissue and than non-attacked plants, indicating that siliciﬁcation is

the stomium, and thereafter fusion of adjacent locules. an inducible defense mechanism against herbivory

Thus, formation of these crystals is believed to aid in [79,80]. For perennial ryegrass (Lolium perenne) and

anther dehiscence and pollen release [19,69]. sheep’s fescue (Festuca ovina), although single attacks

Calcium is required for pollen germination and tube do not alter the silica concentration in the regrowth tissue

growth, and the calcium required is provided by either of either species, repeated attacks by either voles or

the stigma or pollen grains, or both [70,71]. In the anther locusts result in over 400% increases in silica concentra-

of petunia (Petunia hybrida) many calcium crystals ac- tions in both species, and the increases deter attacks by

cumulate under the stomium and adhere to pollen both herbivores [81]. Adverse impacts of silica on herbi-

grains, and they move to the stigma together with pollen vore performance have been reported. Higher silica levels

grains when the anther dehisces and pollen grains are in grasses reduce the growth rates [77,80] and population

released. The increase in calcium concentration on the density [80] of some herbivores; silica-based defenses in

stigma of petunia does not come from the stigma but grasses may play a key role in driving population cycles of

from the calcium crystals adhered to the pollen grains. particular herbivores [80,82], and quantitative heteroge-

Such calcium crystals around the pollen may enhance neity of this plant defense system may contribute to the

pollination by providing calcium required for pollen ger- evolution of high species diversity in herbivores [79].

mination and tube growth of Petunia and Nicotiana [29]. Diatom frustules are remarkably strong to provide me-

To test this hypothesis an extensive survey of the pres- chanical protection for the cells by virtue of their architec-

ence of CaOX crystals in anthers and their relation with ture and the material properties of the silica, and the

the pollination strategies of various plants would need to evolutionary arms-race between diatoms and their spe-

be carried out. cialized predators may have considerable inﬂuence in

structuring pelagic food webs [14].

Ecological signiﬁcance

Herbivore deterrence Contribution to biogeochemical cycles

There is increasing evidence supporting the contention For CaOX biominerals in plants, calcium is taken up from

that biomineralization protects plants against herbivory the soil by roots, and oxalate is biologically synthesized,

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using carbon ﬁxed during photosynthesis, and the original oceanic silicon cycles are driven by recycling of amorphous

source of carbon in biogenic CaOX is therefore atmospheric silica [94]. The role that biogenic amorphous silica plays in

CO2 [2,83,84]. Unlike most carbon-based compounds in the biogeochemical silicon cycle has been discussed in

plants, which break down into their constituent compo- earlier reviews [35,87,94,96].

nents and release CO2 back into the atmosphere when Biosequestration of carbon within phytoliths has been

plants die, CaOX crystals in plants such as the iroko tree reported in a few plant species and/or cultivars, including

(Milicia excelsa) [34,83], the saguaro cactus (Carnegiea economic bamboo species [98], and different wheat (Triti-

gigantea), and other cacti in arid and semi-arid regions cum sp.) [99] and rice (Oryza sativa) [100] cultivars. The

[36,84] are released into the environment and slowly phytolith-occluded carbon is a relatively stable form of

transformed into solid CaCO3 via the oxalate–carbonate organic carbon, it can accumulate in soils after decomposi-

pathway, thus sequestering atmospheric CO2 into the soil tion of plant tissues [101], and it is regarded as a mecha-

as inorganic carbon. The inorganic carbon has a longer soil nism of long-term biogeochemical carbon sequestration

residence time than organic carbon; therefore it is sug- [100].

gested that the bio-induced CaCO3 represents a long-term The above-mentioned biomineralization in plants plays

carbon sink, and the inorganic carbon sink is more efﬁcient an important role in biogeochemical cycling of carbon,

for carbon sequestration than soil organic matter, provided sequestering a signiﬁcant amount of atmospheric CO2.

that the calcium originates from non-carbonate minerals More work is necessary to gain knowledge on the role that

such as calcium-containing silicates [83–85]. In addition, biomineralization in plants may play in mitigating the

when plants mobilize nutrients from silicates in soils, greenhouse effects on global climate change. Crystals of

atmospheric CO2 is consumed and converted to bicarbon- CaOX are widespread in angiosperms, including both

ate, and sequestered in soils as carbonates; even if CO2 is dicotyledons and monocotyledons [102], but biogenic silica

produced when bicarbonate is transformed into carbonate is much more common in monocotyledons, especially in

there is net CO2 sequestration [86–88]. Given that the grasses of the Gramineae family, than in dicotyledons,

formation of CaOX biominerals is common in the plant according to existing literature, and silicon concentrations

kingdom, and that CaCO3 accumulation is observed in soils of monocotyledons (1–15% of shoot dry weight) are gener-

where it is not expected to take place, biomineralization of ally higher than those of most dicotyledons (no more than

CaOX may have locally signiﬁcant impacts upon carbon 0.5% of shoot dry weight) [35]. Studies on the biogeochemi-

and calcium cycling [36,84,86,89]. Biomineralization of cal cycling of carbon, calcium, and silicon in various eco-

CaOX in plants is especially important for the carbon cycle systems with different vegetation types (i.e., vegetation

in arid environments where soil organic carbon contents made up of plants with different accumulation patterns of

are low [36]. calcium and/or silicon biominerals) would further clarify

Coccolithophores play an important role in carbon and the effects of biomineralization on cycling of these ele-

calcium cycling in the oceans. Through photosynthesis and ments, and provide a theoretical basis for ecosystem con-

calciﬁcation, dissolved inorganic carbon is transformed servation and vegetation design of ecosystems that require

into particulate inorganic carbon (CaCO3) and organic restoration.

matter which sink towards the ocean ﬂoor, where cocco-

liths are the largest single component of deep-sea sedi- Concluding remarks and future directions

ments. The precipitation of coccoliths constitutes a sink of In summary, biomineralization is common in plants and

carbon and calcium, although calciﬁcation produces CO2 the chemical composition of biominerals is diverse. Func-

[90,91]. tions of biominerals may depend on their shape, size,

Some studies have demonstrated that biogenic silica is abundance, placement, and chemical composition. In-

an important component of the biogeochemical cycle of creasing evidence supports the physiological signiﬁcance

silicon [35,87,92–97]. Amorphous silica formed in plants of biomineralization in the regulation of cytoplasmic free

can be released into the environment and accumulates in calcium levels, the detoxiﬁcation of aluminum and heavy

soils after plant death because it is more resistant to metals, gathering and scattering light to optimize photo-

decomposition than other plant tissues [93,96]. Dissolved synthesis, and aiding in pollen release, germination, and

silicon released from soil mineral silicates and silica tube growth. The role biomineralization plays in protect-

phytoliths stored in the soil is either taken up by plants ing plants against herbivory and its contribution to the

or transported to rivers and oceans, and used by the biogeochemical cycles of carbon, calcium, and silicon dem-

aquatic ecosystems in which diatoms, the most evident onstrate that biomineralization is also of ecological signif-

biological silicon sink, take up dissolved silicon and de- icance.

posit it as amorphous silica. Rapid recycling of diatom Studying the physiological and ecological signiﬁcance of

silica and silicon import from land are crucial for the biomineralization requires multidisciplinary collabora-

diatom-based food webs [87,94]. Because of its greater tion. Future work should closely link anatomical and

chemical mobility than that of mineral silicates and crys- physiological studies to molecular mechanisms to gain a

talline silica phases, biogenic amorphous silica plays a thorough insight into the physiological signiﬁcance of

major role in the cycling of silicon in soils and aquatic biomineralization. Plant scientists and earth and marine

environments [86,93,94]. It is estimated that the phyto- scientists are expected to join forces to elucidate the role

lith silica ﬁxed annually by terrestrial plants is of the biomineralization plays in ecosystems, especially in se-

same order of magnitude as that ﬁxed in the oceanic questering atmospheric CO2 to mitigate the greenhouse

biogeochemical cycle [35], and both the terrestrial and effects on global climate change.

172

Review Trends in Plant Science March 2014, Vol. 19, No. 3

Acknowledgments 22 Franceschi, V.R. and Schueren, A.M. (1986) Incorporation of

strontium into plant calcium oxalate crystals. Protoplasma 130,

The authors thank John Raven (Dundee University, UK) for critically

199–205

reading an earlier version of this manuscript. This work was supported by

23 Raven, J.A. and Knoll, A.H. (2010) Non-skeletal biomineralization

the Australian Research Council, the Minerals and Energy Research

by eukaryotes: matters of moment and gravity. Geomicrobiol. J. 27,

Institute of Western Australia, Newcrest Mining Ltd. (Telfer Gold Mine),

572–584

and the School of Plant Biology, The University of Western Australia

24 Ernst, W.H.O. et al. (1995) Silicon in developing nuts of the sedge

(UWA). We acknowledge the facilities and scientiﬁc and technical

Schoenus nigricans. J. Plant Physiol. 146, 481–488

assistance of the Australian Microscopy and Microanalysis Research

25 Katayama, H. et al. (2007) Cell wall sheath surrounding calcium

Facility at the Centre for Microscopy, Characterisation and Analysis,

oxalate crystals in mulberry idioblasts. Protoplasma 231, 245–248

UWA, a facility funded by the University and by the State and

26 Lanson, B. et al. (2008) Formation of Zn–Ca phyllomanganate

Commonwealth Governments. Honghua He acknowledges the ﬁnancial

nanoparticles in grass roots. Geochim. Cosmochim. Acta 72,

support by a PhD scholarship jointly awarded by China Scholarship

2478–2490

Council and UWA, funds from the National Natural Science Foundation

27 Rodriguez, N. et al. (2005) Internal iron biomineralization in Imperata

of China (Grant 41301570), and the West China Action Program initiated

cylindrica, a perennial grass: chemical composition, speciation and

by Chinese Academy of Sciences (Grant KZCX2-XB3-13).

plant localization. New Phytol. 165, 781–789

References 28 Sarret, G. et al. (2007) Chemical forms of calcium in Ca,Zn- and Ca,Cd-

containing grains excreted by tobacco trichomes. Can. J. Chem. 85,

1 Bauer, P. et al. (2011) Calcium and silicon mineralization in land

738–746

plants: transport, structure and function. Plant Sci. 180, 746–756

29 Iwano, M. et al. (2004) Calcium crystals in the anther of Petunia: the

2 Franceschi, V.R. and Nakata, P.A. (2005) Calcium oxalate in plants:

existence and biological signiﬁcance in the pollination process. Plant

formation and function. Annu. Rev. Plant Biol. 56, 41–71

Cell Physiol. 45, 40–47

3 Nakata, P.A. (2003) Advances in our understanding of calcium oxalate

30 Currie, H.A. and Perry, C.C. (2007) Silica in plants: biological,

crystal formation and function in plants. Plant Sci. 164, 901–909

biochemical and chemical studies. Ann. Bot. (Lond.) 100, 1383–1389

4 Webb, M.A. (1999) Cell-mediated crystallization of calcium oxalate in

31 Raven, J.A. and Smith, F.A. (1976) Nitrogen assimilation and

plants. Plant Cell 11, 751–761

transport in vascular land plants in relation to intracellular pH

5 Cote´, G.G. (2009) Diversity and distribution of idioblasts producing

regulation. New Phytol. 76, 415–431

calcium oxalate crystals in Dieffenbachia seguine (Araceae). Am. J.

32 Brown, S.L. et al. (2013) Does aridity inﬂuence the morphology,

Bot. 96, 1245–1254

distribution and accumulation of calcium oxalate crystals in Acacia

6 Mazen, A.M.A. et al. (2004) Calcium oxalate formation in Lemna

(Leguminosae: Mimosoideae) ? Plant Physiol. Biochem. 73, 219–228

minor: physiological and ultrastructural aspects of high capacity

33 Raven, J.A. and Giordano, M. (2009) Biomineralization by

calcium sequestration. New Phytol. 161, 435–448

photosynthetic organisms: Evidence of coevolution of the organisms

7 Lersten, N.R. and Horner, H.T. (2011) Unique calcium oxalate ‘duplex’

and their environment? Geobiology 7, 140–154

and ‘concretion’ idioblasts in leaves of tribe Naucleeae (Rubiaceae).

34 Braissant, O. et al. (2004) Biologically induced mineralization in the

Am. J. Bot. 98, 1–11

tree Milicia excelsa (Moraceae): its causes and consequences to the

8 Perez Cuadra, V. and Hermann, P. (2013) Characterization and

environment. Geobiology 2, 59–66

macropattern of calcium oxalate phytoliths in Argentinean endemic

35 Conley, D.J. (2002) Terrestrial ecosystems and the global

species of Chenopodioideae (Amaranthaceae). Quatern. Int. 287, 83–88

biogeochemical silica cycle. Global Biogeochem. Cycles 16, 1121

9 Nitta, I. et al. (2006) Calcium carbonate deposition in a cell wall sac

36 Garvie, L.A.J. (2006) Decay of cacti and carbon cycling.

formed in mulberry idioblasts. Protoplasma 228, 201–208

Naturwissenschaften 93, 114–118

10 Taylor, M.G. et al. (1993) An X-ray absorption spectroscopy study of

37 White, P.J. and Broadley, M.R. (2003) Calcium in plants. Ann. Bot.

the structure and transformation of amorphous calcium carbonate

(Lond.) 92, 487–511

from plant cystoliths. Proc. R. Soc. Lond. B: Biol. Sci. 252, 75–80

38 Kostman, T.A. and Franceschi, V.R. (2000) Cell and calcium oxalate

11 Moore, T.S. et al. (2012) Detection of coccolithophore blooms in ocean

crystal growth is coordinated to achieve high-capacity calcium

color satellite imagery: a generalized approach for use with multiple

regulation in plants. Protoplasma 214, 166–179

sensors. Remote Sens. Environ. 117, 249–263

39 Ruiz, L.P. and Mansﬁeld, T.A. (1994) A postulated role for calcium

12 Dietrich, D. et al. (2003) Silica accumulation in Triticum aestivum L.

oxalate in the regulation of calcium ions in the vicinity of stomatal

and Dactylis glomerata L. Anal. Bioanal. Chem. 376, 399–404

guard cells. New Phytol. 127, 473–481

13 Lins, U. et al. (2002) Structure, morphology, and composition of silicon

40 DeSilva, D.L.R. et al. (1996) Where does all the calcium go? Evidence

biocomposites in the palm tree Syagrus coronata (Mart.) Becc.

of an important regulatory role for trichomes in two calcicoles. Plant

Protoplasma 220, 89–96

Cell Environ. 19, 880–886

14 Hamm, C.E. et al. (2003) Architecture and material properties of

41 Zindler-Frank, E. et al. (2001) Calcium and oxalate content of the

diatom shells provide effective mechanical protection. Nature 421,

841–843 leaves of Phaseolus vulgaris at different calcium supply in relation to

calcium oxalate crystal formation. J. Plant Physiol. 158, 139–144

15 He, H.H. et al. (2012) Morphologies and elemental compositions of

42 Wu, C.C. et al. (2006) Inﬂuence of calcium availability on deposition of

calcium crystals in phyllodes and branchlets of Acacia robeorum

calcium carbonate and calcium oxalate crystals in the idioblasts of

(Leguminosae: Mimosoideae). Ann. Bot. (Lond.) 109, 887–896

Morus australis Poir. leaves. Bot. Stud. 47, 119–127

16 Krejci, M.R. et al. (2011) Selectivity in biomineralization of barium

43 Pennisi, S.V. and McConnell, D.B. (2001) Inducible calcium sinks and

and strontium. J. Struct. Biol. 176, 192–202

preferential calcium allocation in leaf primordia of Dracaena

17 Pritchard, S.G. et al. (2000) Calcium sulfate deposits associated with

sanderiana Hort. Sander ex M. T. Mast. (Dracaenaceae). Hortscience

needle substomatal cavities of container-grown longleaf pine (Pinus

36, 1187–1191

palustris) seedlings. Int. J. Plant Sci. 161, 917–923

44 Franceschi, V.R. (1989) Calcium oxalate formation is a rapid and

18 Storey, R. and Thomson, W.W. (1994) An X-ray microanalysis study of

reversible process in Lemna minor L. Protoplasma 148, 130–137

the salt glands and intracellular calcium crystals of Tamarix. Ann.

45 Volk, G.M. et al. (2002) The role of druse and raphide calcium oxalate

Bot. (Lond.) 73, 307–313

crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant

19 Horner, H.T., Jr and Wagner, B.L. (1980) The association of druse

Biol. 4, 34–45

crystals with the developing stomium of Capsicum annuum

46 Ward, D. et al. (1997) Gazelle herbivory and interpopulation

(Solanaceae) anthers. Am. J. Bot. 67, 1347–1360

differences in calcium oxalate content of leaves of a desert lily. J.

20 He, H.H. et al. (2012) Precipitation of calcium, magnesium, strontium

Chem. Ecol. 23, 333–346

and barium in tissues of four Acacia species (Leguminosae:

47 Ruiz, N. et al. (2002) Calcium oxalate crystals in leaves of Pancratium

Mimosoideae). PLoS ONE 7, e41563

sickenbergeri: constitutive or induced defence? Funct. Ecol. 16, 99–105

21 Monje, P.V. and Baran, E.J. (2005) Evidence of formation of

48 Ernst, W.H.O. (1998) Sulfur metabolism in higher plants: potential for

glushinskite as a biomineral in a Cactaceae species. Phytochemistry

phytoremediation. Biodegradation 9, 311–318

66, 611–614

173

Review Trends in Plant Science March 2014, Vol. 19, No. 3

49 Mazen, A.M.A. (2004) Calcium oxalate deposits in leaves of Corchorus 75 Hudgins, J.W. et al. (2003) Distribution of calcium oxalate crystals in

olitotius as related to accumulation of toxic metals. Russ. J. Plant the secondary phloem of conifers: a constitutive defense mechanism?

Physiol. 51, 281–285 New Phytol. 159, 677–690

50 Mazen, A.M.A. and El Maghraby, O.M.O. (1998) Accumulation of 76 Epstein, E. (2009) Silicon: its manifold roles in plants. Ann. Appl. Biol.

cadmium, lead and strontium, and a role of calcium oxalate in 155, 155–160

water hyacinth tolerance. Biol. Plant. 40, 411–417 77 Massey, F.P. et al. (2006) Silica in grasses as a defence against insect

51 van Balen, E. et al. (1980) Autoradiographic evidence for the herbivores: contrasting effects on folivores and a phloem feeder. J.

incorporation of cadmium into calcium oxalate crystals. Z. Anim. Ecol. 75, 595–603

Pﬂanzenphysiol. 97, 123–133 78 Hunt, J.W. et al. (2008) A novel mechanism by which silica defends

52 Jauregui-Zuniga, D. et al. (2005) Heavy metal stress reduces the grasses against herbivory. Ann. Bot. (Lond.) 102, 653–656

deposition of calcium oxalate crystals in leaves of Phaseolus 79 McNaughton, S.J. and Tarrants, J.L. (1983) Grass leaf siliciﬁcation:

vulgaris. J. Plant Physiol. 162, 1183–1187 natural selection for an inducible defense against herbivores. Proc.

53 Sarret, G. et al. (2006) Trichomes of tobacco excrete zinc as zinc- Natl. Acad. Sci. U.S.A. 80, 790–791

substituted calcium carbonate and other zinc-containing compounds. 80 Massey, F.P. et al. (2008) Are silica defences in grasses driving vole

Plant Physiol. 141, 1021–1034 population cycles? Biol. Lett. 4, 419–422

54 Isaure, M.P. et al. (2010) Calcium promotes cadmium elimination as 81 Massey, F.P. et al. (2007) Herbivore speciﬁc induction of silica-based

vaterite grains by tobacco trichomes. Geochim. Cosmochim. Acta 74, plant defences. Oecologia 152, 677–683

5817–5834 82 Reynolds, J.J.H. et al. (2012) Delayed induced silica defences in

55 Hodson, M.J. and Sangster, A.G. (1993) The interaction between grasses and their potential for destabilising herbivore population

silicon and aluminium in Sorghum bicolor (L.) Moench: growth dynamics. Oecologia 170, 445–456

analysis and X-ray microanalysis. Ann. Bot. (Lond.) 72, 389–400 83 Cailleau, G. et al. (2011) Turning sunlight into stone: the oxalate–

56 Hodson, M.J. and Sangster, A.G. (1998) Mineral deposition in the carbonate pathway in a tropical tree ecosystem. Biogeosciences 8,

needles of white spruce [Picea glauca (Moench.) Voss]. Ann. Bot. 1755–1767

(Lond.) 82, 375–385 84 Garvie, L.A.J. (2003) Decay-induced biomineralization of the saguaro

57 Wang, Y.X. et al. (2004) Apoplastic binding of aluminum is involved in cactus (Carnegiea gigantea). Am. Miner. 88, 1879–1888

silicon-induced amelioration of aluminum toxicity in maize. Plant 85 Cailleau, G. et al. (2004) Biomineralization in plants as a long-term

Physiol. 136, 3762–3770 carbon sink. Naturwissenschaften 91, 191–194

58 Bringezu, K. et al. (1999) Heavy metal tolerance of Silene vulgaris. J. 86 Van Cappellen, P. (2003) Biomineralization and global

Plant Physiol. 154, 536–546 biogeochemical cycles. In Biomineralization (Dove, P.M. et al., eds),

59 Rogalla, H. and Romheld, V. (2002) Role of leaf apoplast in silicon- pp. 357–381, Mineralogical Society of America

mediated manganese tolerance of Cucumis sativus L. Plant Cell 87 Street-Perrott, F.A. and Barker, P.A. (2008) Biogenic silica: a

Environ. 25, 549–555 neglected component of the coupled global continental

60 da Cunha, K.P.V. and do Nascimento, C.W.A. (2009) Silicon effects on biogeochemical cycles of carbon and silicon. Earth Surf. Process.

metal tolerance and structural changes in maize (Zea mays L.) grown Landforms 33, 1436–1457

on a cadmium and zinc enriched soil. Water Air Soil Pollut. 197, 88 Raven, J.A. and Edwards, D. (2001) Roots: evolutionary origins and

323–330 biogeochemical signiﬁcance. J. Exp. Bot. 52, 381–401

61 Neumann, D. and zur Nieden, U. (2001) Silicon and heavy metal 89 Borrelli, N.L. et al. (2009) Calcium biominerals in typical Argiudolls

tolerance of higher plants. Phytochemistry 56, 685–692 from the Pampean Plain, Argentina: an approach to the

62 Hodson, M.J. and Evans, D.E. (1995) Aluminium–silicon interactions understanding of their role within the calcium biogeochemical

in higher plants. J. Exp. Bot. 46, 161–171 cycle. Quatern. Int. 193, 61–69

63 Liang, Y. et al. (2007) Mechanisms of silicon-mediated alleviation of 90 Bernard, O. et al. (2008) Multimodel analysis of the response of the

abiotic stresses in higher plants: a review. Environ. Pollut. 147, 422–428 coccolithophore Emiliania huxleyi to an elevation of pCO2 under

64 Franceschi, V.R. and Horner, H.T., Jr (1980) Calcium oxalate crystals nitrate limitation. Ecol. Model. 211, 324–338

in plants. Bot. Rev. 46, 361–427 91 von Dassow, P. et al. (2012) Calciﬁcation state of coccolithophores can

65 Franceschi, V. (2001) Calcium oxalate in plants. Trends Plant Sci. 6, be assessed by light scatter depolarization measurements with ﬂow

331 cytometry. J. Plankton Res. 34, 1011–1027

66 Kuo-Huang, L.L. et al. (2007) Correlations between calcium oxalate 92 Derry, L.A. et al. (2005) Biological control of terrestrial silica cycling

crystals and photosynthetic activities in palisade cells of shade- and export ﬂuxes to watersheds. Nature 433, 728–731

adapted Peperomia glabella. Bot. Stud. 48, 155–164 93 Alexandre, A. et al. (1997) Plant impact on the biogeochemical cycle of

67 Gal, A. et al. (2012) Certain biominerals in leaves function as light silicon and related weathering processes. Geochim. Cosmochim. Acta

scatterers. Adv. Mater. 24, OP77–OP83 61, 677–682

68 Balch, W.M. et al. (1996) The 1991 coccolithophore bloom in the 94 Struyf, E. and Conley, D.J. (2008) Silica: an essential nutrient in

central North Atlantic .1. Optical properties and factors affecting wetland biogeochemistry. Front. Ecol. Environ. 7, 88–94

their distribution. Limnol. Oceanogr. 41, 1669–1683 95 Fulweiler, R.W. and Nixon, S.W. (2005) Terrestrial vegetation and the

69 Horner, H.T. and Wagner, B.L. (1992) Association of four seasonal cycle of dissolved silica in a southern New England coastal

different calcium crystals in the anther connective tissue and river. Biogeochemistry 74, 115–130

hypodermal stomium of Capsicum annuum (Solanaceae) during 96 Clarke, J. (2003) The occurrence and signiﬁcance of biogenic opal in

microsporogenesis. Am. J. Bot. 79, 531–541 the regolith. Earth Sci. Rev. 60, 175–194

70 Ge, L.L. et al. (2007) Calcium function and distribution during 97 Farmer, V.C. et al. (2005) The role of phytolith formation and

fertilization in angiosperms. Am. J. Bot. 94, 1046–1060 dissolution in controlling concentrations of silica in soil solutions

71 Ge, L.L. et al. (2009) Distribution of calcium in the stigma and style of and streams. Geoderma 127, 71–79

tobacco during pollen germination and tube elongation. Sex. Plant 98 Parr, J. et al. (2010) Carbon bio-sequestration within the phytoliths of

Reprod. 22, 87–96 economic bamboo species. Global Change Biol. 16, 2661–2667

72 Korth, K.L. et al. (2006) Medicago truncatula mutants demonstrate 99 Parr, J.F. and Sullivan, L.A. (2011) Phytolith occluded carbon and

the role of plant calcium oxalate crystals as an effective defense silica variability in wheat cultivars. Plant Soil 342, 165–171

against chewing insects. Plant Physiol. 141, 188–195 100 Li, Z. et al. (2013) Occluded C in rice phytoliths: implications to

73 Molano-Flores, B. (2001) Herbivory and calcium concentrations affect biogeochemical carbon sequestration. Plant Soil 370, 615–623

calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann. 101 Parr, J.F. and Sullivan, L.A. (2005) Soil carbon sequestration in

Bot. (Lond.) 88, 387–391 phytoliths. Soil Biol. Biochem. 37, 117–124

74 Ruiz, N. et al. (2002) Responses of Pancratium sickenbergeri to 102 Prychid, C.J. and Rudall, P.J. (1999) Calcium oxalate crystals in

simulated bulb herbivory: combining defence and tolerance monocotyledons: a review of their structure and systematics. Ann.

strategies. J. Ecol. 90, 472–479 Bot. (Lond.) 84, 725–739

174