JXB Advance Access originally published online on March 31, 2003
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Journal of Experimental Botany, Vol. 54, No. 386, pp. 1431-1446,
May 1, 2003
© 2003 Oxford University Press
Variation in the shoot calcium content of angiosperms
Received 11 October 2002; Accepted 16 January 2003
Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK
1 To whom correspondence should be addressed. Fax: +44 (0)1789 470552. E-mail: martin.broadley{at}hri.ac.uk
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionAppendix 1References |
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This study describes the variation in the mean relative shoot Ca content within the angiosperms at the ordinal level. Data were derived from studies in the literature in which the shoot Ca content of two or more species had been compared, and from a hydroponic experiment in which plants were selected to represent the relative number of species within each angiosperm order. Across all angiosperms, most of the variation in shoot Ca content occurred at and above the level of the order. Relative shoot Ca contents and variances correlated between literature and experimental data. In general, orders of commelinoid monocots had lower Ca contents than other monocot or eudicot orders. These results are used to illustrate how physiological and ecological hypotheses can be formulated using literature data.
Key words: Calcium, cation, nutrient-film technique (NFT), plant mineral content, residual maximum likelihood (REML) analyses, phylogeny.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendix 1References |
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Angiosperms (flowering plants) diverged from non-flowering seed plants 120 million years ago (APG, 1998). There are 200–250 thousand extant species of angiosperms, the majority of which map to one of 47 monophyletic orders (Fig. 1a; APG, 1998; Soltis et al., 1999; Kuzoff and Gasser, 2000). Over 75% of angiosperm species occur in 12 species-rich orders (Fig. 1b). These are the monocot orders Poales and Asparagales (e.g. grass and orchid species, respectively), and the eudicot orders Asterales (e.g. sunflower), Caryophyllales (e.g. beet), Ericales (e.g. heather), Fabales (e.g. bean), Gentianales (e.g. coffee), Lamiales (e.g. mint), Malpighiales (e.g. cassava), Myrtales (e.g. Fuchsia), Rosales (e.g. strawberry), and Sapindales (e.g. Citrus).
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Calcium is an essential and major plant nutrient, which fulfils a variety of structural and messenger roles. The Ca2+ cation is required extracellularly to maintain cell wall and membrane structure and within the vacuole as a counter-cation for inorganic and organic anions (White, 1998). In the cytoplasm Ca2+ is required for signalling and explicit perturbations in Ca2+ concentration ([Ca2+]cyt) link specific environmental or developmental stimuli to their appropriate physiological responses (Sanders et al., 1999; Knight, 2000; White, 2000). A submicromolar [Ca2+]cyt is maintained to prevent interference with cell metabolism and [Ca2+]cyt is buffered by Ca2+-chelating organic compounds that are present in millimolar concentrations. Shoot Ca content varies between 0.1% and 5% on a dry weight basis, depending on species and growth conditions (Marschner, 1995).
Calcium is acquired by the plant root system from the soil solution. Shoot Ca content is determined by the rates of root uptake, sequestration within root vacuoles and upward translocation in the xylem. Calcium may traverse the root to the xylem through either the interconnected cytoplasm of root cells (symplast) or through the extracellular spaces (apoplast). The identity and/or activity of proteins catalysing Ca2+ transport across root cell membranes might influence Ca2+ fluxes through the symplastic pathway. Structural characteristics, such as the cell wall cation-exchange capacity (CEC), and transpiration rates might influence Ca2+ fluxes through the apoplastic pathway (White, 2001). Root CEC could also influence Ca2+ fluxes through the symplast by affecting the effective cation concentrations at the extracellular face of the plasma membrane of root cells. It has been speculated that the greater shoot Ca content of dicots (
eudicots) than monocots, may be due to the greater CEC of their roots (Asher and Ozanne, 1961; Crooke and Knight, 1962; Marschner, 1995; Thompson et al., 1997).
It has been estimated that up to half of the total variation in leaf Ca content occurs at the phylogenetic division between eudicots and monocots (Thompson et al., 1997). Phylogenetic differences in shoot Ca contents have not been resolved at lower taxonomic levels, although three distinct ‘physiotypes’ for Ca nutrition have been postulated, and these are exemplified by particular plant families (Kinzel, 1982). The recognized physiotypes are ‘oxalate plants’ that precipitate Ca as the oxalate salt, as exemplified by certain families of the Caryophyllales and Malpighiales, ‘calciotrophes’ that contain high concentrations of free Ca2+, as exemplified by certain families of the Brassicales (e.g. cabbage) and Fabales, and ‘potassium plants’ that have a high K/Ca ratio, as exemplified by families in the Apiales (e.g. carrot) and Asterales.
Phylogenetic variation in shoot mineral contents can be determined using data compiled from the literature. Such analyses have been performed for Cs (Broadley et al., 1999) and heavy metals (Broadley et al., 2001). For example, eudicot orders generally have higher shoot Ni and Zn contents than monocot orders, and over 40% of the variation in shoot content of Ni and Zn occurs at the level of order or above. Variation in plant mineralogies at this scale may reflect phylogenetically-constrained root and shoot anatomies, morphologies and/or ion transport processes (Broadley et al., 2001; White et al., 2002b). However, literature data sets are phylogenetically unbalanced since they are comprised mainly of crop plants and botanical curiosities and may not provide accurate estimates of phylogenetic effects.
The aim of this work was to determine the variation in the shoot Ca content of angiosperms and to test the suitability of using phylogenetically unbalanced data from the literature. Thus (i) the shoot Ca content of angiosperm orders was determined from data available in the literature, (ii) the shoot Ca content of angiosperm orders was determined from an experiment in which species were sampled in proportion to the frequency of species within that order, and (iii) the data from the experiment and literature were compared.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendix 1References |
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This study comprised three components: a literature survey, a glasshouse experiment, and a comparison of literature and experimental approaches. A recent angiosperm phylogeny (APG, 1998; Soltis et al., 1999) was used to partition the variation in the Ca content of plant shoots.
Literature survey
Selecting primary data: Primary data were obtained from papers in which direct comparisons of shoot Ca contents were made in two or more angiosperm species. Papers were chosen in which species were grown under the same conditions either in solution culture or in the same substrate. Papers based on field or herbarium samples, or based on plant collections from natural habitats, whose mineral nutrition had not been controlled, were excluded. Within each paper, different treatments (e.g. different external Ca concentrations; [Ca2+]ext) were considered as independent comparative studies. All studies were included, unless plants had been stressed with a severe nutrient deficiency or toxicity other than [Ca2+]ext (e.g. salinity or a metal stress such as Al or Fe toxicity). When more than one subspecies, cultivar, variety, accession or morphotype of the same species was used in a study, a mean value was used. Data were taken for leaves, when available, or for entire shoots. A set of 61 papers (Appendix 1), representing 244 comparative studies, were identified in which at least one plant species was contained within another study, and in which no subsets of unlinked data arose.
Generating comparative data using residual maximum likelihood analyses: The original data from the 244 studies were subjected to a residual maximum likelihood (REML) analysis (Thompson and Welham, 2000), using a procedure described previously (Broadley et al., 1999, 2001). Briefly, this procedure adjusted for differences in between-study means to generate a mean relative shoot Ca content for the 206 plant species represented in the 244 studies. Estimates of variation in shoot Ca content were assigned between and within the following groups: informal plant division (n=3; eudicot, commelinoid monocot, non-commelinoid monocot), order (n=19) and species (n=206) using both REML analyses and hierarchical, nested analyses of variance (ANOVA). All statistical analyses were performed using GenStat (Fifth Edition, Release 4.2, VSN International, Oxford, UK).
Phylogenetically-designed experiment
Background: Estimating the mean shoot Ca content of angiopserm orders would ideally involve sampling all species within all orders as discussed by Broadley et al. (2001). Since this is clearly impractical, a proportional sampling regime was designed to ensure that the whole phylogeny was fairly represented and to minimize bias. To determine the number of species to be selected from each order, ordinal species distributions were determined using a web-based approach. The Angiosperm Phylogeny Group (APG, 1998) ordinal classification, provided by the ‘Flowering Plant Gateway’ (http://www.csdl.tamu.edu/FLORA/newgate/gateopen.htm, Texas AandM Bioinformatics Working Group, Texas, USA), was used as a framework to access a database of angiosperm families systematically (http://biodiversity.uno.edu/delta/angio/index.htm, Watson and Dallwitz, 1991, 1992 onwards). The numbers of species within an order were calculated as the sum of the family totals. The total number of angiosperm species, assigned to monophyletic orders, was estimated to be 195 493 using this approach. The number of species from any given order selected for this study was proportional to the frequency of species in that order within all angiosperm species. So, for example, since the Caryophyllales contains 10 214 species, 5.2% of the species selected for this study were chosen from this order.
Once the numbers of species to be sampled from each order was determined, the second consideration was that all species within a particular order, family or genus should have an equal probability of selection. However, obtaining and culturing species selected totally at random was impractical. Thus, a within-order selection criteria was adopted as follows: first, species were selected according to the frequency of species in each family. This ensured that species selection favoured families containing large numbers of species. Second, species were selected according to the commercial availability of their seeds. This was achieved by identifying a single seed company who could supply a sufficiently diverse range of seeds suitable for growing in the environmental conditions outlined in the next section (Chiltern Seeds, Ulverston, Cumbria, UK). The choice of species was thus restricted to the 5000 taxa offered by this company, although several species of crops representing commercially-used cultivars were also used. The taxa used in this study are therefore biased towards the 65 000 named taxa sold for horticulture in the UK (Crawley et al., 1996).
Plant material: Two hundred species of (mainly herbaceous) angiosperms were obtained. Seeds were weighed prior to germination. Large seeds were imbibed in deionized water overnight. All other seeds were sown in Petri dishes on the surface of filter paper moistened with deionized water. Following imbibition, large seeds were sown in Petri dishes between two circles of filter paper moistened with deionized water. Seeds were germinated in the dark, either at 25 °C, or at 4 °C. For several species, mould appeared on seeds during germination and seeds were re-sown in sterile conditions, following soaking in 10% NaOCl for 6 min. Once a radicle was observed, individual seedlings were transplanted to rockwool plugs (2.5x2.5x4 cm; Grodan, Hedehusene, Denmark) and watered with tap water in plastic trays. The plastic trays were covered with plastic film to maintain humidity, and placed in a weaning room held at 25 °C. Three to five days after transplanting, rockwool plugs were transferred to the hydroponic system in the glasshouse.
Hydroponic system and glasshouse: The experiment was carried out between July and October 2001 in a 40 m2 glasshouse compartment at Wellesbourne, UK (latitude 52°12'18'' N, longitude 1°36'00'' W, 48.8 m above sea level). The glasshouse was set to maintain temperatures of 25 °C by day and 15 °C at night using automatic vents and supplementary heating. The hydroponic system adopted was nutrient film technique (NFT). The system comprised 12 individual gullies (5.15 m length x 0.11 m width x 0.05 m depth) constructed from flat-bottomed PVC guttering. The gullies were spaced 0.26 m apart (centre-to-centre) in two groups of six within the same glasshouse compartment. Seventy-two holes, each of a sufficient size to contain two rockwool plugs (diameter 4.5 cm), were cut at equal distances (every 6 cm) along 4.32 m strips of PVC. One of these strips was secured to the top of each gully and the remaining 0.83 m of guttering was covered with a separate strip of PVC containing no holes. Two rockwool plugs were placed in each hole so that their bases rested directly on the bottom of the gully. Each gully was connected to one of two water-storage tanks that each contained 200 l of deionized water to which mineral nutrient salts were added. The nutrient solutions contained 2 mM Ca(NO3)2, 2 mM NH4NO3, 0.75 mM MgSO4, 0.5 mM KOH, 0.25 mM KH2PO4, 0.1 mM FeNaEDTA, 30 µM H3BO3, 25 µM CaCl2, 10 µM MnSO4, 3 µM CuSO4, 1 µM ZnSO4, 0.5 µM Na2MoO4. Nutrient solutions were adjusted daily to pH 6, using H2SO4, and solutions were replaced completely twice a week. The nutrient solutions were pumped from the supply tanks to the top-end of the gullies. Subsequently, the nutrient solutions flowed along the bottom of the gullies under the influence of gravity (the gradient was <2°) and drained back into the tanks. The flow rates were controlled using taps to ensure that the nutrient solutions flowed in a thin layer (c. 2 mm in depth) along the bottom of each gully. As plants were sampled during the experiment, the resulting gaps in the PVC strips were immediately covered to maintain humidity and to reduce algal growth in the gullies.
Experimental design: The NFT system was designed so that 12 gullies ran along a north–south axis, each gully consisting of 72 units (positions for plants). A Latinized alpha design was used to allocate six replicates of 144 species in blocks of 12 units, each gully containing six blocks. This design ensured that pairs of species occurred together within a block at most once over the whole design. Each of six pairs of adjacent gullies contained a complete replicate of the 144 species. Further, each species occurred at most twice in each of six blocks of 12 plant positions along the gullies. Thus, the experimental design allowed adjustments for spatial variability in both the north–south and east–west axes and provided the most efficient comparison of species possible. Two rockwool plugs were placed within each hole to allow duplicate plants to be grown, that were bulked for mineral analyses. In all, 117 species germinated sufficiently well for plugs to be transplanted to their designated hole. To determine if the 117 species were phylogenetically balanced, species distributions from each order were compared to the species distributions across all angiosperms. The phylogenetic distribution of the 117 species used in this study approximated the phylogenetic distribution of all species (Fig. 2).
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Analyses of plant shoots: Shoots were separated into leaves and stems where possible and fresh weights were recorded. Duplicate samples from each experimental unit were bulked and dried in paper bags for 72 h in a fan-assisted oven set to 80 °C. The dry weights of leaves and stems were measured and dry tissue was subsequently milled to a powder using a ball-mill. Total Ca measurements were obtained from dry leaf tissue using the micro Kjeldahl method, with c. 0.1 g subsamples of dried plant material digested for 1 h following addition of 1 ml of H2O2 and 2 ml of a H2SO4/Se catalyst (Bradstreet, 1965). Inductively-coupled plasma emission spectrophotometry (JY24, Jobin-Yvon ISA, France) was used to determine Ca concentrations in digested material. Estimates of variation in shoot Ca content were assigned between and within the following groups: (replicate/gully) x block, informal plant division (n=3; eudicot, commelinoid monocot, non-commelinoid monocot), order plus one unassigned family (n=25) and species (n=117) using REML analyses and hierarchical, nested analyses of variance (ANOVA). All statistical analyses were performed using GenStat.
Comparison of literature and experimental approaches
Mean shoot Ca contents derived from the literature survey and from the experiment were compared. Comparisons were made at the informal group, the order and at the species levels using correlation analyses. Variances associated with the trait of shoot Ca content were estimated using REML between and within each informal group, and between and within each order, restricted for each informal group. Proportions of variance associated with hierarchical structures were compared between literature and experimental data using correlation analyses. Within-order variances in shoot Ca content were estimated after restricting for order.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendix 1References |
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The mean relative shoot Ca content of 206 species derived from the literature (Table 1) ranged between –0.75 (Triticum durum, Poales) and 5.62 (Cucumis sativus, Cucurbitales). These data are relative values on a linear scale and negative values can arise from the REML fitting procedures (Thompson and Welham, 2000). The seed fresh weight, duration of growth, shoot fresh and dry weights at harvest, and the mean shoot Ca content of 117 species grown in the phylogenetically-designed experiment, are presented in Table 2. The mean shoot Ca content of species sampled in the experiment ranged between 0.11% Ca (Phoenix canariensis, Arecales) and 4.41% Ca (Brassica oleracea, Brassicales). The trait of shoot Ca content was approximately normally distributed for literature and experimental data (Fig. 3).
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The mean relative shoot Ca content of 19 orders derived from the literature (Table 3) ranged between –0.01 (Ericales, eudicot) and 3.19 (Cucurbitales, eudicot). The mean shoot Ca content of the 24 orders and one unassigned family represented in the experiment ranged between 0.07% Ca (Arecales, commelinoid monocot) and 3.29% Ca (Cucurbitales, eudicot). In general, orders with low mean shoot Ca were Arecales and Poales (both commelinoid monocots), and the eudicot orders Ericales, Myrtales and Malpighiales. Orders with high mean shoot Ca were the eudicot orders Cucurbitales, Brassicales, Malvales, and Rosales.
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The literature survey and the experiment had three informal groups, 15 orders and 33 species in common (Fig. 4). Literature and experimental data were related at both the informal group, ordinal and species levels. There was a highly significant correlation between the mean shoot Ca content of orders (r=0.74; df=13; P <0.01) and species (r=0.45; df=31; P <0.01) derived from literature and experimental data. The two species that were conspicuously high in Ca content in the experiment, as compared to the literature, were Brassica oleracea and Cucurbita maxima.
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Estimates of variance in shoot Ca content between and within each informal group, and between and within each order restricting for informal group, are presented in Table 4. The proportion of variance accounted for at the level of order and above was 54.5% for the literature data and 63.8% for the experimental data. Within the eudicots and the commelinoid monocots, the proportion of variance accounted for at the level of order and above was 14.8% and 65.3%, respectively, from the literature data. For the experimental data, the corresponding figures were higher (38.3% and 77.5%, respectively). Estimates of variance in shoot Ca content, expressed as a percentage of the total variance occurring within each of the restricted subsets (Table 4), yield a positive correlation between the literature and experimental data (r=0.77; df=5; P <0.05). Further, there were contrasting patterns of within-order variance in shoot Ca content between different orders. The Poales had low within-order variance in shoot Ca content in both literature and experimental data. By contrast, the Brassicales had high within-order variance in shoot Ca content. Well-represented orders with intermediate levels of within-order variance in shoot Ca content included the Asterales and Fabales.
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Discussion |
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Phylogenetic scope
This work is the first step in a sampling strategy to determine the phylogenetic influence on a continuous trait (Broadley et al., 2001). It was designed both to estimate the shoot Ca content of angiosperm orders and to validate phylogenetically unbalanced data from the literature. Across all angiosperms, the majority of the variation in shoot Ca content occurred at the level of order and above and, in general, the shoot Ca contents of eudicot orders were greater than those of monocot orders. Informal groups, orders and species common to both the literature and experimental data had Ca contents and variance structures which correlated. Thus, across all angiosperms, phylogenetically unbalanced data from the literature yielded comparable information to a phylogenetically balanced experiment.
The work described here allows trait variance components to be quantified and assigned at informal group and order levels. However, it does not allow variance components to be resolved within orders since this would require more species to be surveyed. To estimate the variation within 44 of the 47 angiosperm orders simultaneously (excluding the three orders with fewest species, Acorales, Ceratophyllales, and Garryales, with 6, 10 and 24 species, respectively) would require at least three species to be selected from the order with least species (Cornales, 465 species) and pro rata sampling of orders for a further c. 1300 species. Clearly data are not available for these species in the literature and experiments cannot be performed on this number of species easily. Practically, the collection of sufficient data may never be phylogenetically balanced (Broadley et al., 2001). However, two feasible approaches could allow trait variance components from biased and non-biased species distributions to be compared through simulation, which would allow the validity of analysing incomplete data sets to be tested with greater rigour. Both approaches rely on the accumulation of large data sets. The first approach would be to integrate data from different parts of the phylogeny using standard experiments performed in different laboratories or at different times. Once enough data were collected, within-order variance components could be estimated using both phylogenetically-biased and non-biased sampling simulations. The second approach would be to collect leaf material from a living botanical collection, although these data could be compromised by substrate heterogeneity. In this context, it is noteworthy that a distinct phylogenetic influence on leaf Ca content was reported amongst plants in their natural habitats (Thompson et al., 1997). Notwithstanding the uncertain estimates of within-order variation, the work described here demonstrates that substantial information can be obtained from the literature to guide the selection of phylogenetic regions for further experimental probing, either through comparative experiments or through ecological surveys.
Differences in shoot Ca content between orders
In general, the shoot Ca contents of eudicot orders were greater than those of monocot orders. Within the monocots, low shoot Ca contents were associated with commelinoid monocots. In addition to the Poales, commelinoid monocots include the orders Zingiberales, Commelinales, Arecales, and the unassigned family Dasypogonaceae. The non-commelinoid monocots include the orders Asparagales, Liliales, Pandanales, Dioscoreales, Alismatales, Acorales, and the unassigned family Petrosaviaceae. The hypothesis that differences in shoot Ca content occur between commelinoid and non-commelinoid monocots could be tested explicitly using a sampling strategy designed specifically for these groups, using the logic outlined in this paper. Ideally species would be sampled pro rata from all monocot orders (53 419 species). Since the monocot order with the fewest species is the Acorales (six species), half of all monocot species would need to be sampled to yield at least three species from each order. This selection of species would be dominated by the families Poaceae (12 000 species) and Orchidaceae (17 000 species) in the orders Poales (commelinoid) and Asparagales (non-commelinoid), respectively. A more pragmatic approach to testing the hypothesis that differences in shoot Ca content occur between commelinoid and non-commelinoid monocots may be to restrict comparisons to the families Poaceae and Orchidaceae, or to experiment on species-rich and species-poor clades on separate occasions. Within the eudicots, derived orders within both the rosid and the asterid clades had the highest shoot Ca contents. These included the Cucurbitales, Rosales, Malvales, and Brassicales in the rosids, and the Apiales, Asterales, Lamiales, and Solanales in the asterids. Again, the hypothesis that differences in shoot Ca content occur between these derived orders and other closely-related orders could be tested explicitly using a sampling strategy designed specifically for these groups.
Hypotheses can be formulated to account for the differences in shoot Ca content between orders. Since shoot Ca content is determined principally by the rate of Ca uptake, its sequestration in the root vacuoles and its loading into the xylem, differences in either the activities of proteins that transport Ca2+ across cell membranes or in the relative contributions of symplastic (cytoplasmic) and apoplastic (extracellular) pathways to the movement of Ca to the xylem might impact on shoot Ca content (White, 2001). Differences in the activity of Ca2+ transporters is an attractive proposition, especially since Arabidopsis mutants lacking specific plasma membrane Ca2+ channels have been shown to have reduced shoot Ca content (White et al., 2002a).
Differences in shoot Ca content between monocots and eudicots have traditionally been attributed to the CEC of the root, based on correlative evidence (Asher and Ozanne, 1961; Crooke and Knight, 1962; Marschner, 1995). The root CEC is located in the apoplast, and is attributed to the free carboxyl groups of galacturonic acids of cell wall pectins in the middle lamella (Haynes, 1980; Sattelmacher, 2001). Within the monocots, the pectin contents of shoot cell walls, which are comparable to those of root cell walls, are low to intermediate in commelinoid monocots whilst the pectin content of shoot cell walls is similar to dicots in the non-commelinoid monocots (Jarvis et al., 1988). Commelinoid monocots had lower shoot Ca contents than non-commelinoid monocots in this study. Thus, the traits of root CEC, pectin content of shoot cell walls, and shoot Ca content may correlate. Mechanistically, since fixed negative charges and charge screening can influence both the absolute and relative extracellular cation concentrations, root CEC could determine shoot Ca content by affecting the rate and selectivity of Ca uptake into the symplast and/or Ca transport through the apoplast (Asher and Ozanne, 1961; Wacquant, 1977). This hypothesis could be tested through comparative experiments on species from parts of the monocot phylogeny that differ in their shoot Ca content.
Calcium metabolism
Differences in shoot Ca contents between orders might also be due to differences in their ‘Ca2+-metabolism’. This term describes the consequences of the chemical equilibria occurring between Ca2+ and different organic and inorganic complexes. Since [Ca2+]cyt above low micromolar levels is extremely toxic, plants tend to sequester Ca2+ into vacuolar, endoplasmic reticular or cytoplasmic complexes. Taxonomic differences in Ca2+-metabolism occur within the angiosperms. For example, most taxa deposit Ca oxalate crystals within their cells, although this is most prevalent in families in the order Caryophyllales, including the Polygonaceae, Chenopodiaceae, Caryophyllaceae, and Cactaceae (Kinzel, 1982; Monje and Baran, 2002). Within the monocots, Ca oxalate crystals are absent from only the commelinoid monocots Juncaceae and Cyperaceae (Prychid and Rudall, 1999; Monje and Baran, 2002). Several eudicot families, notably the Brassicaceae (Brassicales) and Crassulaceae (Rosales) do not mineralize appreciable quantities of Ca oxalate, but instead accumulate significant quantities of water-soluble Ca complexes in their vacuoles (Kinzel, 1982; Kinzel and Lechner, 1992). The selective advantages of different Ca-metabolism strategies are speculative. For example, the distinct mineralogies of taxa in the Caryophyllales may reflect an ancestral selection pressure of highly mineralized substrates in dry environments (Ehrendorfer, 1976; Cuénoud et al., 2002). A further set of taxa with distinct mineralogies is the ‘potassium-plants’. These plants contain little mineralized or water-soluble Ca (Kinzel, 1982) and occur in the families Apiaceae (Apiales), Campanulaceae and Asteraceae (Asterales). Contrasting Ca metabolisms may explain the differences in shoot Ca content of angiosperms, and may also be the reason why certain mineral elements are correlated either positively (e.g. Broadley et al., 2001), or negatively (e.g. commelinoid monocots can accumulate significant amounts of silicon in their shoots; Epstein, 1999).
Using knowledge of the phylogenetic distributions of continuous traits
Discrete traits are used routinely to formulate plant taxonomies and information is readily available in the literature. Thus, distinct floral (Soltis et al., 2002) and endosperm (Williams and Friedman, 2002) anatomies have been used to formulate hypotheses amenable to physiological and genetic dissection (Soltis et al., 2002). Data on continuous traits are less readily available. However, when sufficient data are compiled, it is clear that the phylogenetic position of a species influences many continuous traits, such as plant lifespan, age at sexual maturity, generation time (Franco and Silvertown, 1996), seed weight (Hodgson and Mackey, 1986; Westoby et al., 1995), and plant mineral content (Broadley et al., 1999, 2001; Jansen et al., 2002). In addition to formulating physiological hypotheses, elucidating the phylogenetic effects impacting on shoot mineralogy has several other uses. First, since shoot mineralogies are correlated with ecological traits (Thompson et al., 1997; Grime, 2001), it may be possible to improve predictions of the responses of plant communities to environmental change using phylogenetic information. Second, shoot mineralogies of higher phylogenetic levels can aid the prediction of the relative transport of minerals from soils to the shoots of plant species whose transfer coefficients are not known and thereby improve nutrient cycling and contaminant transfer models (Broadley et al., 2001). Third, defining the phylogenetic impact on the mineral content of plants is important for predicting human dietary mineral intakes. For example, commelinoid monocots (e.g. rice, cereals, maize, and bananas) constitute a large proportion of the human diet for much of the world’s population and are likely to be a relatively poor source of Ca. Knowing the genetic potential for increasing the Ca content of edible portions of commelinoid monocots such as rice and cereals could inform plant-breeding strategies to alleviate Ca-deficiency disorders in populations reliant upon these crops (Graham et al., 2001).
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Acknowledgements |
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The authors wish to thank Mark Powell and Simon Elliott, for plant mineral analyses, Edward Tucker, for experimental help, and Duncan Greenwood and Graham Seymour for comments on the manuscript. HLC was supported by a Rank Prize Funds Vacation Studentship. JPH was supported by an HRI Browning Studentship. The research in our laboratories is supported principally by the Biotechnology and Biological Sciences Research Council (UK) and by the Department for Environment, Food and Rural Affairs (UK).
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Appendix 1 |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendix 1References |
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