Phylogenetic Variation in the Silicon Composition of Plants

Abstract

INTRODUCTION

Silicon is the second most abundant element in the soil after oxygen (reviewed by Epstein, 1999; Richmond and Sussman, 2003). Most Si is present in the soil as insoluble oxides or silicates, although soluble silicic acid occurs in the range of 0·1–0·6 mm. Silicon is also one of the most abundant mineral elements in plant tissues and shoot concentrations in excess of 10 % d. wt have been reported (Epstein, 1999). Plants growing under natural conditions do not appear to suffer from Si deficiencies. However, Si-containing fertilizers are routinely applied to several crops including rice (Pereira et al., 2004) and sugar cane (Savant et al., 1999) to increase crop yield and quality. Increased Si supply improves the structural integrity of crops and may also improve plant tolerance to diseases, drought and metal toxicities (reviewed by Epstein, 1999; Richmond and Sussman, 2003; Ma, 2004). For example, Si deposition in the cell walls of root endodermal cells may contribute to the maintenance of an effective apoplastic barrier and thereby improve plant resistance to disease and drought stresses (Lux et al., 2002, 2003a, b; Hattori et al., 2005), whilst intra- and extracellular deposition of aluminosilicates in roots and shoots is thought to protect some species from potential Al toxicity (Hodson and Evans, 1995; Hodson and Sangster, 1999; Britez et al., 2002; Jansen et al., 2003; Wang et al., 2004).

Early studies of Si in plants noted that species of Poaceae contained between 10 and 20 times the concentration of Si found in non-monocotyledonous species (de Saussure, 1804; Jones and Handreck, 1967). Recent reviews report that Si accumulation is, in general, higher in monocot than in non-monocot species (Epstein, 1999; Richmond and Sussman, 2003). However, detailed sampling of specimens from botanical gardens by Takahashi and colleagues (reviewed in Ma and Takahashi, 2002, and references therein) indicates that Si accumulation is largely restricted to primitive land plants and to certain monocot clades, namely the Poaceae, Cyperaceae and Commelinaceae. There is also evidence from these detailed studies that Si may accumulate in certain dicot clades such as the Urticaceae and Cucurbitaceae. In this study, the phylogenetic variation in shoot Si concentration amongst plant species has been quantified by analysing all of the appropriate literature data that could be sourced. These include the extensive data compiled by Takahashi and colleagues (Ma and Takahashi, 2002, and references therein). Using a recent consensus angiosperm phylogeny, it was thus possible to test the hypothesis that high shoot Si concentration is a general feature of monocot species, and it was also possible to identify Si accumulation features in several other well-represented clades of plant species.

MATERIALS AND METHODS

Data from 125 studies, contained in 54 papers in the primary literature, were identified that reported Si concentrations of leaf or non-woody shoot tissues in at least two species growing in the same environment, and which contained at least one species in common with another study (studies listed in the Appendix; additional information is available online at http://aob.oxfordjournals.org). Wherever possible, species nomenclature was based on the original study. Where taxonomic uncertainties occurred, the closest species match was inferred. Angiosperm species nomenclature and familial assignment/informal groupings were based on the United States Department of Agriculture (USDA) National Genetic Resources Program. Germplasm Resources Information Network (GRIN) (http://www.ars-grin.gov/cgi-bin/npgs/html/index.pl) and the Angiosperm Phylogeny Group classification (APG, 1998). Non-angiosperm species nomenclature and family assignment was based on information obtained from (a) The Flowering Plant Gateway (http://www.csdl.tamu.edu/FLORA/newgate/gateopen.htm); (b) The International Plant Names Index (http://www.ipni.org/index.html); or (c) The National Center for Biotechnology Information (NCBI; http://www.ncbi.nlm.nih.gov).

The mean relative shoot Si concentration of each species across all studies was estimated. To adjust for differences in shoot Si concentration between studies, a residual maximum likelihood (REML) procedure was used. All methods have been described previously (Broadley et al., 2003). Briefly, the REML procedure adjusts for differences in between-study variances and means in order to generate an overall treatment mean, which in this case is the shoot Si concentration for each species, i.e. species means are effectively averaged across studies. Since the REML fitting procedures can produce negative treatment means, species Si concentrations were considered as relative values on a linear scale. Estimates of variation in shoot Si concentration were simultaneously fit to a variance components model of [study+(group/order/family/genus/species)]. To test for significant differences between species classified by their higher-level phylogenetic position, one-way ANOVA was performed on restricted subsets of the data. All statistical analyses were performed using GenStat (Release 6.1.0.200, VSN International, Oxford, UK).

RESULTS AND DISCUSSION

Seven hundred and thirty-five species were sampled from 125 studies (Table 1; additional information is available online at http://aob.oxfordjournals.org), including 600 species of angiosperms, 67 gymnosperms, 59 ferns (Polypodiophyta), five clubmosses (Lycopodiophyta), two horsetails (Equisetophyta), one liverwort (Marchantiophyta) and one moss (Bryophyta). Within a variance components model of [study+(group/order/family/genus/species)], group and order accounted for 67 % of the variation in relative shoot Si concentration (Table 2). The remaining variation was attributed to within-order (17 %) and to between-study (16 %) variance components. Thus, high-level phylogenetic position influences the shoot Si concentration of plants. This observation is consistent with literature and experimental studies of other elements including Ca, K, Mg (Broadley et al., 2003, 2004; White and Broadley, 2003; White, 2005), Ni and Zn (Broadley et al., 2001). In contrast, variation in the relative shoot concentrations of N, P (Broadley et al., 2004) and Se (White et al., 2004) is dominated by species-level variance components, and thus there is no evidence that the tissue concentration of these elements differs systematically between groups of species according to their phylogenetic position.

Table 1.

Mean relative shoot Si concentration of 735 plant species. Data are from 125 studies, contained in 54 papers in the primary literature, in which Si concentrations of leaf or non-woody shoot tissue were reported. Each study included at least two plant ...

Table 2.

Variance components model of shoot Si concentrations, based on a meta-analysis of primary data from 125 studies, contained in 54 papers in the primary literature, in which Si concentrations of leaf or non-woody shoot tissue were reported

Across all plant species, relative shoot Si concentration varied from −2·139 in Colysis wrightii (Polypodiaceae) to 8·769 in Arundinaria gigantea (Poaceae); the mean was 0·722 (Table 1 and Fig. 1). Negative relative shoot Si concentration values can arise as a consequence of adjusting for between-study variation during REML fitting procedures. Mean relative shoot Si concentrations of some fern species from the study of Ma and Takahashi (2002) formed a distinct distribution peak in the low relative shoot Si concentration range (Fig. 1, inset). However, since the mean relative shoot Si concentrations adjusted for differences between studies using the REML procedure corresponded closely to the arithmetic mean shoot Si concentration across all studies (Fig. 2), and since there was a minimal ‘study’ variance component (Table 2), data from Ma and Takahashi (2002) were retained in subsequent analyses.

Fig. 1.

Ranked mean relative shoot Si concentration in 735 species of plants based on data from 125 independent studies in 54 papers in the primary literature. A residual maximum likelihood (REML) procedure was used to adjust for differences in shoot Si concentration ...

Fig. 2.

The arithmetic mean shoot Si concentration as a function of mean relative shoot Si concentration, adjusted for differences in shoot Si concentration between studies using a residual maximum likelihood (REML) procedure. Data are based on 125 independent ...

Mean relative shoot Si concentrations differed significantly between the seven groups of plant species [one-way ANOVA, F_6,728 = 18·11, P < 0·001, residual mean square (r.m.s.) = 1·053; Fig. 3]. Shoot Si concentration declined in the order liverworts > horsetails > clubmosses >mosses > angiosperms > gymnosperms > ferns. Notable Si accumulators included Equisetaceae species Equisetum arvense (3·992) and Equisetum hyemale (2·917). However, non-vascular plant species were poorly represented in this study and any inferences about the general Si biology of these groups are not possible without further representation in the analysis.

Fig. 3.

Mean (± s.e.m.) relative shoot Si concentration of seven groups of plants (one-way ANOVA, F_6,728 = 18·11, P < 0·001, residual mean square = 1·053). Silicon concentrations in leaf or non-woody shoot tissues of 735 ...

Relative shoot Si concentrations were, in general, low in angiosperms, gymnosperms and ferns. However, there was substantial variation in shoot Si concentration within these well-represented groups. The 59 species of ferns sampled in this study were assigned to 14 families representing seven orders (Table 1). The relative shoot Si concentration of ferns ranged from −2·139 in Colysis wrightii (Polypodiaceae) to 1·352 in Athyrium filix-femina (Woodsiaceae). Although there were no significant differences in mean relative shoot Si concentration between fern orders (one-way ANOVA, F_6,52 = 1·29, P > 0·05, r.m.s. = 2·448), there were differences in the mean relative shoot Si concentration between the seven fern families sampled from the best-represented fern order (Aspleniales; one-way ANOVA, F_6,36 = 4·27, P < 0·01, r.m.s. = 2·729). There were notable differences in relative shoot Si concentration between species in the Woodsiaceae (0·59, n = 11) and in the Dryopteridaceae (–1·68, n = 19).

The 67 species of gymnosperms sampled in this study were assigned to nine families representing five orders (Table 1). The relative shoot Si concentration of gymnosperms ranged from −0·078 in Ephedra sinica (Ephedraceae) to 4·512 in Abies pectinata (Pinaceae). There were no significant differences in mean relative shoot Si concentration between gymnosperm orders (one-way ANOVA, F_4,62 = 0·46, P > 0·05, r.m.s. = 0·387). Further, there were no significant differences in the mean relative shoot Si concentration between the five gymnosperm families sampled from the best-represented gymnosperm order (Pinales; one-way ANOVA, F_4,56 = 0·01, P > 0·05, r.m.s. = 0·428). In the three well-represented families from this order, mean relative shoot Si concentrations were 0·333 (Taxodiaceae, n = 6), 0·379 (Cupressaceae, n = 10) and 0·387 (Pinaceae, n = 43).

The 600 species of angiosperms sampled in this study were assigned to 114 families of plants representing 44 orders/families unassigned to order (Table 1). These comprised 34 non-monocot and ten monocot (five commelinoid and five non-commelinoid) clades. Mean relative shoot Si concentrations differed significantly between these 44 clades (one-way ANOVA, F_43,556 = 5·17, P < 0·001, r.m.s. = 0·76; Fig. 4). Within non-monocot angiosperms, notable low relative shoot Si concentrations occurred amongst Brassicales (0·010, n = 9), Aquifoliales (0·102, n = 3), Cornales (0·196, n = 4) and Fabales (0·263, n = 36) species. High relative shoot Si concentrations were observed in species of Saxifragales (1·351, n = 5), with notable Si accumulation in two species of Crassulaceae (Rhodiola linearifolia, 2·679; Sedum hybridum, 3·329). High relative shoot Si concentrations were also observed in several species of Fagales (0·786, n = 25) including Fagus sylvatica (6·089) and Quercus spp. from the Fagaceae family, in the Rosales (0·764, n = 25) including species from the Celtidaceae, Elaeagnaceae, Ulmaceae and Urticaceae families, in the Asterales (e.g. Helianthus spp.), and in the Caryophyllales (Polygonum spp.). There was intermediate-to-high relative shoot Si concentration in the basal angiosperm groups, although these groups were poorly represented in the analysis (Magnoliales 0·578, n = 4; Laurales 0·592, n = 4; Piperales 0·617, n = 2; Nymphaeaceae 0·685, n = 1; Schisandraceae 1·209, n = 1).

Fig. 4.

Mean (±s.e.m.) relative shoot Si concentration in 44 angiosperm clades (representing orders or unassigned families; one-way ANOVA, F_43,556 = 5·17, P < 0·001, residual mean square = 0·76). Data were obtained from ...

Within monocots, shoot Si concentration was substantially lower in non-commelinoid monocot species than in commelinoid monocots (Fig. 5). Indeed, three of the four angiosperm orders containing the lowest shoot Si concentrations were the non-commelinoid monocot orders Acorales (–0·028, n = 2), Liliales (0·055, n = 3) and Asparagales (0·081, n = 24). In contrast, the well-replicated commelinoid monocot orders Arecales (1·204, n = 9) and Poales (1·554, n = 189) had consistently high relative shoot Si concentrations. The few species sampled from other commelinoid monocot clades had low relative shoot Si concentrations, similar to species in non-commelinoid monocot clades, e.g. species of Bromeliaceae (0·199, n = 2) and Commelinales (0·292, n = 1). Thus, from the available data in the published literature, it is concluded that high shoot Si concentration is not a general feature of monocots.

Fig. 5.

Percentage frequency distribution of mean relative shoot Si concentration of 600 species of angiosperms classified into commelinoid monocot (continuous line), non-commelinoid monocot (dashed line), or non-monocot (dotted line) groupings.

The main products of Si accumulation are the phytoliths, or silica bodies, which infill the cell walls and lumina of certain cells in plant tissues (Prychid et al., 2004). The shapes and sizes of these phytoliths contain considerable taxonomic information (Powers, 1992; Prychid et al., 2004) and are increasingly being used in both palaeoecological (e.g. Parker et al., 2004) and archaeological (e.g. Ishida et al., 2003) research, since they provide useful information on past vegetation, agriculture and food. Notably, Prychid et al. (2004), working on phytolith systematics in monocots, suggested that silica accumulation was confined to the commelinoid monocots, with the single exception of the Orchidaceae. Since Piperno (1988, tables 2.2–2.4) found that phytolith production was closely related to plant Si content, the observation of Prychid et al. (2004) is consistent with this analysis of published shoot Si data, subject to the caveat that only two Orchidaceae species were represented in the present data set. Thus, this analysis of published shoot Si data indicates which phylogenetic groups are most likely to contain species that are good phytolith producers. Further, this analysis also indicates that shoot Si content, and thus phytolith production, will be influenced more by the higher-level phylogenetic position of a plant rather than by environmental effects such as water availability, temperature, and Si availability in the soil, although environmental effects will influence phytolith production under some circumstances (e.g. Rosen and Weiner, 1994).

In addition to providing useful potential palaeoecological and archaeological information, knowledge of phylogenetic variation in shoot Si accumulation may also inform studies of the biogeochemical cycling of Si, and those of the molecular genetics of Si uptake and transport in plants. For example, Carnelli et al. (2001) estimated the annual contribution of alpine plant communities to the Si biogeochemical cycle in alpine environments and, unsurprisingly, observed that grasslands were the greatest silica producers. Relative Si production in other plant communities could be estimated by multiplying the mean relative shoot Si concentration of each plant phylogenetic grouping represented (e.g. plant family), by the percentage abundance for each group.

To date, Si transporters have only been located in diatoms (Hildebrand et al., 1997). However, rice (a heavy Si accumulator with a mean relative shoot Si concentration of 4·167) has recently become a model plant for the study of Si uptake and transport in vascular plants (Ma et al., 2002, 2004; Mitani and Ma, 2005). Since a rice mutant with markedly decreased Si uptake compared with its wild type has recently been identified (Ma et al., 2002), it seems likely that Si transporter(s) in higher plants will be isolated in due course. The present data will facilitate comparative functional genetic analysis of these transporters (e.g. Mitani and Ma, 2005), by allowing closely related target species with contrasting Si accumulation patterns to be identified for gene/trait association analysis.

There are many phylogenetic groups of plant species that are not represented in this study. To remedy this, further field surveys or comparative experiments are needed and potential sampling strategies are described in Broadley et al. (2003). In the case of Si, field surveys are likely to yield more appropriate information than laboratory experiments for two reasons. First, it has been shown that relative shoot Ca and Mg data are broadly consistent between experimental and field conditions (Broadley et al., 2003, 2004). Since plant-available soil Si is likely to vary less than plant-available soil Ca and Mg between sites, and since there is a relatively small effect of site on relative shoot Si concentration, it is a reasonable (and testable) assumption that field data will correspond in relative terms to comparative experimental data. The second reason is that it is easier and cheaper to sample large numbers of species from their natural habitats—or from botanical collections—than to grow them experimentally from seeds or cuttings. Once further data are collected, it will be possible (1) to determine precisely where Si accumulation traits diverge within commelinoid monocots, (2) to test which of the non-vascular plant groups are characterized by high Si accumulation, and (3) to identify if distinct ordinal/family-level Si accumulation traits occur in groups of species not currently represented in the present data set.

SUPPLEMENTARY INFORMATION

Online at http://aob.oxfordjournals.org provides raw shoot/leaf Si concentrations on a dry weight basis of 735 plant species sampled from 125 studies, contained in 54 papers in the primary literature (full references in the Appendix), in which Si concentrations of leaf or non-woody shoot tissue were reported.

APPENDIX

This Appendix provides data sources for meta-analysis to calculate mean relative shoot Si concentration in plants. Study numbers, in square brackets, are cited in Table 1 and in Supplementary Information.

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Supplementary Material

Acknowledgments

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